Abstract
This study aimed to evaluate the effects of low-energy red light-emitting diode (LED) irradiation on the proliferation and osteogenic differentiation of periodontal ligament stem cells (PDLSCs). PDLSCs were derived from human periodontal ligament tissues of premolars and were irradiated with 0 (control group), 1, 3, or 5 J/cm2 red LED in osteogenic induction medium. Cell proliferation was analyzed using the 3-[4,5-dimethylthiazol-2-yl]-2,5 diphenyl tetrazolium bromide (MTT) assay. Osteogenic differentiation activity was evaluated by monitoring alkaline phosphatase (ALP) activity, alizarin red staining, and real-time polymerase chain reaction (RT-PCR) results. Osteoblast-associated proteins (Runx2, OCN, OPN, and BSP) were detected using western blotting. The results of the MTT assay indicated that PDLSCs in the irradiation groups exhibited a higher proliferation rate than those in the control group (P < 0.05). ALP results showed that after 7 days of illumination, only 5 J/cm2 promoted the expression of ALP of PDLSCs. However, after 14 days of illumination, the irradiation treatments did not increase ALP activity. The results of alizarin red staining showed that red LED promoted osteogenic differentiation of the PDLSCs. The real-time polymerase chain reaction (RT-PCR) results demonstrated that red LED upregulated the expression levels of osteogenic genes. Expression of the proteins BSP, OPN, OCN, and Runx2 in the irradiation groups was higher than that in the control group. Our results confirmed that low-energy red LED at 1, 3, and 5 J/cm2 promotes proliferation and osteogenic differentiation of PDLSCs.
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References
Sun HY, Jiang H, Du MQ, Wang X, Feng XP, Hu Y, Lin HC, Wang B, Si Y, Wang CX, Zheng SG, Liu XN, Rong WS, Wan WJ, Tai BJ (2018) The prevalence and associated factors of periodontal disease among 35 to 44-year-old Chinese adults in the 4th National Oral Health Survey. Chin J Dent Res 21(4):241–247. https://doi.org/10.3290/j.cjdr.a41082
Sculean A, Nikolidakis D, Nikou G, Ivanovic A, Chapple IL, Stavropoulos A (2015) Biomaterials for promoting periodontal regeneration in human intrabony defects: a systematic review. Periodontol 68(1):182–216. https://doi.org/10.1111/prd.12086
de Freitas LF, Hamblin MR (2016) Proposed mechanisms of photobiomodulation or low-level light therapy. IEEE J Select Top Quantum Electron 22(3):7000417. https://doi.org/10.1109/JSTQE.2016.2561201
Li Y, Zhang J, Xu Y, Han Y, Jiang B, Huang L, Zhu H, Xu Y, Yang W, Qin C (2016) The histopathological investigation of red and blue light emitting diode on treating skin wounds in Japanese big-ear white rabbit. PLoS One 11(6):e0157898. https://doi.org/10.1371/journal.pone.0157898
Peng F, Wu H, Zheng Y, Xu X, Yu J (2012) The effect of noncoherent red light irradiation on proliferation and osteogenic differentiation of bone marrow mesenchymal stem cells. Lasers Med Sci 27(3):645–653. https://doi.org/10.1007/s10103-011-1005-z
Tao CY, Lee N, Chang HC, Yang C, Yu XH, Chang PC (2016) Evaluation of 660 nm LED light irradiation on the strategies for treating experimental periodontal intrabony defects. Lasers Med Sci 31(6):1113–1121. https://doi.org/10.1007/s10103-016-1958-z
Sohn HM, Ko Y, Park M, Kim B, Park JE, Kim D, Moon YL, Lim W (2017) Comparison of the alendronate and irradiation with a light-emitting diode (LED) on murine osteoclastogenesis. Lasers Med Sci 32(1):189–200. https://doi.org/10.1007/s10103-016-2101-x
Lee G, Kim B, Ko Y, Park M, Kim D, Ryu KH, Jun YC, Sohn HM, Lim W (2017) Regulation of RANKL-induced osteoclastogenesis by 635-nm light-emitting diode irradiation via HSP27 in bone marrow-derived macrophages. Photomed Laser Surg 35(2):78–86. https://doi.org/10.1089/pho.2016.4134
Gu X, Li M, Jin Y, Liu D, Wei F (2017) Identification and integrated analysis of differentially expressed lncRNAs and circRNAs reveal the potential ceRNA networks during PDLSC osteogenic differentiation. BMC Genet 18(1):100. https://doi.org/10.1186/s12863-017-0569-4
Zhu T, Wu Y, Zhou X, Yang Y, Wang Y (2019) Irradiation by blue light-emitting diode enhances osteogenic differentiation in gingival mesenchymal stem cells in vitro. Lasers Med Sci 34(7):1473–1481. https://doi.org/10.1007/s10103-019-02750-3
Sun X, Lou L, Zhong K, Wan L (2017) MicroRNA-451 regulates chemoresistance in renal cell carcinoma by targeting ATF-2 gene. Exp Biol Med (Maywood NJ) 242(12):1299–1305. https://doi.org/10.1177/1535370217701625
Yang ZH, Zhang XJ, Dang NN, Ma ZF, Xu L, Wu JJ, Sun YJ, Duan YZ, Lin Z, Jin Y (2009) Apical tooth germ cell-conditioned medium enhances the differentiation of periodontal ligament stem cells into cementum/periodontal ligament-like tissues. J Periodontal Res 44(2):199–210. https://doi.org/10.1111/j.1600-0765.2008.01106.x
Gao Y, Zhao G, Li D, Chen X, Pang J, Ke J (2014) Isolation and multiple differentiation potential assessment of human gingival mesenchymal stem cells. Int J Mol Sci 15(11):20982–20996. https://doi.org/10.3390/ijms151120982
Mamalis A, Jagdeo J (2015) Light-emitting diode-generated red light inhibits keloid fibroblast proliferation. Dermatol Surg 41(1):35–39. https://doi.org/10.1097/01.DSS.0000452650.06765.51
Babaee A, Nematollahi-Mahani SN, Shojaei M, Dehghani-Soltani S, Ezzatabadipour M (2018) Effects of polarized and non-polarized red-light irradiation on proliferation of human Wharton's jelly-derived mesenchymal cells. Biochem Biophys Res Commun 504(4):871–877. https://doi.org/10.1016/j.bbrc.2018.09.010
Feng R, Morine Y, Ikemoto T, Imura S, Iwahashi S, Saito Y, Shimada M (2018) Photobiomodulation with red light-emitting diodes accelerates hepatocyte proliferation through reactive oxygen species/extracellular signal-regulated kinase pathway. Hepatol Res 48(11):926–936. https://doi.org/10.1111/hepr.13182
Asai T, Suzuki H, Kitayama M, Matsumoto K, Kimoto A, Shigeoka M, Komori T (2014) The long-term effects of red light-emitting diode irradiation on the proliferation and differentiation of osteoblast-like MC3T3-E1 cells. Kobe J Med Sci 60(1):E12–E18
Yang D, Yi W, Wang E, Wang M (2016) Effects of light-emitting diode irradiation on the osteogenesis of human umbilical cord mesenchymal stem cells in vitro. Sci Rep 6:37370. https://doi.org/10.1038/srep37370
Horvát-Karajz K, Balogh Z, Kovács V, Drrernat AH, Sréter L, Uher F (2009) In vitro effect of carboplatin, cytarabine, paclitaxel, vincristine, and low-power laser irradiation on murine mesenchymal stem cells. Lasers Surg Med 41(6):463–469. https://doi.org/10.1002/lsm.20791
Parker S (2007) Low-level laser use in dentistry. Br Dent J 202(3):131–138. https://doi.org/10.1038/bdj.2007.75
Fekrazad R, Asefi S, Allahdadi M, Kalhori KA (2016) Effect of photobiomodulation on mesenchymal stem cells. Photomed Laser Surg 34(11):533–542. https://doi.org/10.1089/pho.2015.4029
Pagin MT, de Oliveira FA, Oliveira RC, Sant'Ana AC, de Rezende ML, Greghi SL, Damante CA (2014) Laser and light-emitting diode effects on pre-osteoblast growth and differentiation. Lasers Med Sci 29(1):55–59. https://doi.org/10.1007/s10103-012-1238-5
Mamalis A, Garcha M, Jagdeo J (2015) Light emitting diode-generated blue light modulates fibrosis characteristics: fibroblast proliferation, migration speed, and reactive oxygen species generation. Lasers Surg Med 47(2):210–215. https://doi.org/10.1002/lsm.22293
Mandrillo PM, Fischetto G, Odorisio P, Cura F, Avantaggiato A, Carinci F (2017) Effects of light-emitting diode (led 640 nm) on human gingival fibroblasts: a comparative in vitro study. ORAL Implantol 10(2):151–161. https://doi.org/10.11138/orl/2017.10.2.151
Yamauchi N, Taguchi Y, Kato H, Umeda M (2018) High-power, red-light-emitting diode irradiation enhances proliferation, osteogenic differentiation, and mineralization of human periodontal ligament stem cells via ERK signaling pathway. J Periodontol 89(3):351–360. https://doi.org/10.1002/JPER.17-0365
Holder MJ, Milward MR, Palin WM, Hadis MA, Cooper PR (2012) Effects of red light-emitting diode irradiation on dental pulp cells. J Dent Res 91(10):961–966. https://doi.org/10.1177/0022034512456040
Green DE, Longtin JP, Sitharaman B (2009) The effect of nanoparticle-enhanced photoacoustic stimulation on multipotent marrow stromal cells. ACS Nano 3(8):2065–2072. https://doi.org/10.1021/nn900434p
Klionsky DJ, Emr SD (1989) Membrane protein sorting: biosynthesis, transport and processing of yeast vacuolar alkaline phosphatase. EMBO J 8(8):2241–2250
Saberi E, Farhad-Mollashahi N, Sargolzaei Aval F, Saberi M (2019) Proliferation, odontogenic/osteogenic differentiation, and cytokine production by human stem cells of the apical papilla induced by biomaterials: a comparative study. Clin Cosmet Investig Dent 11:181–193. https://doi.org/10.2147/CCIDE.S211893
Kim HK, Kim JH, Abbas AA, Kim DO, Park SJ, Chung JY, Song EK, Yoon TR (2009) Red light of 647 nm enhances osteogenic differentiation in mesenchymal stem cells. Lasers Med Sci 24(2):214–222. https://doi.org/10.1007/s10103-008-0550-6
Liu YK, Uemura T, Nemoto A, Yabe T, Fujii N, Ushida T, Tateishi T (1997) Osteopontin involvement in integrin-mediated cell signaling and regulation of expression of alkaline phosphatase during early differentiation of UMR cells. FEBS Lett 420(1):112–116. https://doi.org/10.1016/s0014-5793(97)01498-1
Vahabi S, Torshabi M, Esmaeil Nejad A (2016) In vitro comparison of the efficacy of TGF-β1 and PDGF-BB in combination with freeze-dried bone allografts for induction of osteogenic differentiation in MG-63 osteoblast-like cells. J Mater Sci Mater Med 27(12):182. https://doi.org/10.1007/s10856-016-5802-6
Stein A, Benayahu D, Maltz L, Oron U (2005) Low-level laser irradiation promotes proliferation and differentiation of human osteoblasts in vitro. Photomed Laser Surg 23(2):161–166. https://doi.org/10.1089/pho.2005.23.161
Funding
This work was supported by the Luzhou Municipal People’s Government-Southwest Medical University science and technology strategic cooperation projects of China (no. 2017LZXNYD-T03), Luzhou Municipal Science and Technology Bureau of China (no. 2016-R-70(13/24)). The reagents of this study were supported by these funds that all came from Southwest Medical University.
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All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Yan Wu and Tingting Zhu. The first draft of the manuscript was written by Yan Wu and Tingting Zhu, and all authors commented on previous versions of the manuscript. The authors read and approved the final manuscript.
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All procedures performed in the study were in accordance with the Ethics Committee of the Affiliated Hospital of Stomatology Southwest Medical University Certificate (contract grant 20180314001) and with the 1964 Declaration of Helsinki and its later amendments or comparable ethical standards.
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Yan Wu and Tingting Zhu contributed to the work equally and regarded as co-first authors.
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Wu, Y., Zhu, T., Yang, Y. et al. Irradiation with red light-emitting diode enhances proliferation and osteogenic differentiation of periodontal ligament stem cells. Lasers Med Sci 36, 1535–1543 (2021). https://doi.org/10.1007/s10103-021-03278-1
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DOI: https://doi.org/10.1007/s10103-021-03278-1