Abstract
Increasing interest has been observed in the use of photobiomodulation (PBM) to enhance the proliferation of stem cells and induce their differentiation. The effects of PBM at two different wavelengths (635 and 809 nm) with three different energy densities (0.5, 1 and 2 J/cm2) on the osteogenic differentiation of adipose-derived stem cells (ADSC) were investigated. Cell viability and proliferation were evaluated by MTT and Alamar Blue assays. Osteoblast differentiation were assessed by alkaline phosphatase (ALP) activity, Alizarin red staining and reverse-transcription polymerase chain reaction (RT-PCR) for the expression of collagen type I (COL1A), ALP and osteocalcin. 635 nm and 809 nm laser irradiation had no effect on the cell viability on days 7 and 14, except for 0.5 J/cm2 group at 14th day after 635 nm irradiation (p < 0.05). Cell proliferation was not changed significantly. Mineralization was increased significantly in 809 nm laser groups but no enhancement was detected in the osteogenic differentiation by ALP activity and gene expression results. In 0.5 and 1 J/cm2 groups, ALP and COL1A expressions were down regulated at day 7 after 809 nm laser exposure. These results suggest that PBM may alter osteogenic differentiation of ADSC and increase mineralization but further investigation is needed to define adequate parameters.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abrahamse H (2009) The use of laser irradiation to stimulate adipose derived stem cell proliferation and differentiation for use in autologous grafts. AIP Conf Proc 1172:95–100. https://doi.org/10.1063/1.3250132
Abrahamse H (2011) Inducing stem cell differentiation using low intensity laser irradiation: a possible novel therapeutic intervention. Cent Eur J Biol 6:695–698. https://doi.org/10.2478/s11535-011-0068-y
Abramovitch-Gottlib L, Gross T, Naveh D et al (2005) Low level laser irradiation stimulates osteogenic phenotype of mesenchymal stem cells seeded on a three-dimensional biomatrix. Lasers Med Sci 20:138–146. https://doi.org/10.1007/s10103-005-0355-9
Al-Nasiry S, Hanssens M, Luyten C, Pijnenborg R (2007) The use of alamar blue assay for quantitative analysis of viability, migration and invasion of choriocarcinoma cells. Hum Reprod 22:1304–1309. https://doi.org/10.1093/humrep/dem011
Amaroli A, Agas D, Laus F et al (2018) The effects of photobiomodulation of 808 nm diode laser therapy at higher fluence on the in vitro osteogenic differentiation of bone marrow stromal cells. Front Physiol 9:1–11. https://doi.org/10.3389/fphys.2018.00123
Amid R, Kadkhodazadeh M, Ahsaie MG, Hakakzadeh A (2014) Effect of low level laser therapy on proliferation and differentiation of the cells contributing in bone regeneration. J Lasers Med Sci 5:163–170
Amini AR, Laurencin CT, Nukavarapu SP (2012) Bone tissue engineering: recent advances and challenges. Crit Rev Biomed Eng 40:363–408. https://doi.org/10.1615/critrevbiomedeng.v40.i5.10
Anders JJ, Lanzafame RJ, Arany PR (2015) Low-level light/laser therapy versus photobiomodulation therapy. Photomed Laser Surg. https://doi.org/10.1089/pho.2015.9848
Anders JJ, Arany PR, Baxter GD, Lanzafame RJ (2019) Light-emitting diode therapy and low-level light therapy are photobiomodulation therapy. Photobiomodu Photomed Laser Surg 37:63–65. https://doi.org/10.1089/photob.2018.4600
Anwer AG, Gosnell ME, Perinchery SM et al (2012) Visible 532 nm laser irradiation of human adipose tissue-derived stem cells: effect on proliferation rates, mitochondria membrane potential and autofluorescence. Lasers Surg Med 44:769–778. https://doi.org/10.1002/lsm.22083
Ateş GB, Ak A, Garipcan B, Gülsoy M (2017) Methylene blue mediated photobiomodulation on human osteoblast cells. Lasers Med Sci 32:1847–1855. https://doi.org/10.1007/s10103-017-2286-7
Ateş GB, Ak A, Garipcan B, Gülsoy M (2018) Indocyanine green-mediated photobiomodulation on human osteoblast cells. Lasers Med Sci 33:1591–1599. https://doi.org/10.1007/s10103-018-2530-9
Bölükbaşı Ateş G, Ak Can A, Gülsoy M (2017) Investigation of photobiomodulation potentiality by 635 and 809 nm lasers on human osteoblasts. Lasers Med Sci 32:591–599. https://doi.org/10.1007/s10103-017-2153-6
Bouvet-Gerbettaz S, Merigo E, Rocca J-P et al (2009) Effects of low-level laser therapy on proliferation and differentiation of murine bone marrow cells into osteoblasts and osteoclasts. Lasers Surg Med 41:291–297. https://doi.org/10.1002/lsm.20759
Bunnell BA, Flaat M, Gagliardi C et al (2008) Adipose-derived stem cells: isolation, expansion and differentiation. Methods 45:115–120. https://doi.org/10.1016/j.ymeth.2008.03.006
Caetano GF, Bártolo PJ, Domingos M et al (2015) Osteogenic differentiation of adipose-derived mesenchymal stem cells into Polycaprolactone (PCL) scaffold. Procedia Engin. 110:59–66
Choi K, Kang B-J, Kim H et al (2013) Low-level laser therapy promotes the osteogenic potential of adipose-derived mesenchymal stem cells seeded on an acellular dermal matrix. J Biomed Mater Res B Appl Biomater 101:919–928. https://doi.org/10.1002/jbm.b.32897
de Andrade ALM, Luna GF, Brassolatti P et al (2019) Photobiomodulation effect on the proliferation of adipose tissue mesenchymal stem cells. Lasers Med Sci 34:677–683. https://doi.org/10.1007/s10103-018-2642-2
De Freitas LF, Hamblin MR (2016) Proposed mechanisms of photobiomodulation or low-level light therapy. IEEE J Sel Top Quantum Electron 22:348–364. https://doi.org/10.1109/jstqe.2016.2561201
de Oliveira TS, Serra AJ, Manchini MT et al (2014) Effects of low level laser therapy on attachment, proliferation, and gene expression of VEGF and VEGF receptor 2 of adipocyte-derived mesenchymal stem cells cultivated under nutritional deficiency. Lasers Med Sci 30:217–223. https://doi.org/10.1007/s10103-014-1646-9
de Villiers JA, Houreld NN, Abrahamse H (2011) Influence of low intensity laser irradiation on isolated human adipose derived stem cells over 72 h and their differentiation potential into smooth muscle cells using retinoic acid. Stem Cell Rev 7:869–882. https://doi.org/10.1007/s12015-011-9244-8
Deana AM, de Souza AM, Teixeira VP et al (2018) The impact of photobiomodulation on osteoblast-like cell: a review. Lasers Med Sci 33:1147–1158. https://doi.org/10.1007/s10103-018-2486-9
Engler AJ, Sen S, Sweeney HL, Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 126:677–689. https://doi.org/10.1016/j.cell.2006.06.044
Fekrazad R, Asefi S, Eslaminejad MB et al (2019) Photobiomodulation with single and combination laser wavelengths on bone marrow mesenchymal stem cells: proliferation and differentiation to bone or cartilage. Lasers Med Sci 34:115–126. https://doi.org/10.1007/s10103-018-2620-8
Ferreira MP, Ferrari RA, Gravalos ED, Martins MD, Bussadori SK, Gonzalez DA, Fernandes KP (2009) Effect of low-energy gallium-aluminum-arsenide and aluminium gallium indium phosphide laser irradiation on the viability of C2C12 myoblasts in a muscle injury model. Photomed Laser Surg 27:901–906. https://doi.org/10.1089/pho.2008.2427
Frese L, Dijkman PE, Hoerstrup SP (2016) Adipose tissue-derived stem cells in regenerative medicine. Transfus Med, Hemotherapy
Fujihara NA, Hiraki KRN, Marques MM (2006) Irradiation at 780 nm increases proliferation rate of osteoblasts independently of dexamethasone presence. Lasers Surg Med 38:332–336. https://doi.org/10.1002/lsm.20298
Gerlier D, Thomasset N (1986) Use of MTT colorimetric assay to measure cell activation. J Immunol Methods 94:57–63. https://doi.org/10.1016/0022-1759(86)90215-2
Ginani F, Soares DM, Barreto e V MP, Barboza CAG (2015) Effect of low-level laser therapy on mesenchymal stem cell proliferation: a systematic review. Lasers Med Sci 30:2189–2194. https://doi.org/10.1007/s10103-015-1730-9
Green DE, Longtin JP, Sitharaman B (2009) The effect of nanoparticle-enhanced photoacoustic stimulation on multipotent marrow stromal cells. ACS Nano 3:2065–2072. https://doi.org/10.1021/nn900434p
Gregory CA, Gunn WG, Peister A, Prockop DJ (2004) An Alizarin red-based assay of mineralization by adherent cells in culture: comparison with cetylpyridinium chloride extraction. Anal Biochem 329:77–84. https://doi.org/10.1016/j.ab.2004.02.002
Grottkau BE, Lin Y (2013) Osteogenesis of adipose-derived stem cells. Bone Res. 1:133–145
Halvorsen YD, Franklin D, Bond AL et al (2001) Extracellular matrix mineralization and osteoblast gene expression by human adipose tissue-derived stromal cells. Tissue Eng 7:729–741. https://doi.org/10.1089/107632701753337681
Hawkins D, Abrahamse H (2006) Effect of multiple exposures of low-level laser therapy on the cellular responses of wounded human skin fibroblasts. Photomed Laser Surg 24:705–714. https://doi.org/10.1089/pho.2006.1076
Hoemann CD, El-Gabalawy H, McKee MD (2009) In vitro osteogenesis assays: influence of the primary cell source on alkaline phosphatase activity and mineralization. Pathol Biol (Paris) 57:318–323. https://doi.org/10.1016/j.patbio.2008.06.004
Huang Y-Y, Chen AC-H, Carroll JD, Hamblin MR (2009) Biphasic dose response in low level light therapy. Dose Response 7:358–383. https://doi.org/10.2203/dose-response.09-027.hamblin
Huang Y-Y, Sharma SK, Carroll J, Hamblin MR (2011) Biphasic dose response in low level light therapy—an update. Dose Response 9:602–618. https://doi.org/10.2203/dose-response.11-009.hamblin
Jawad MM, Husein A, Azlina A et al (2013) Effect of 940 nm low-level laser therapy on osteogenesis in-vitro. J Biomed Opt 18:128001. https://doi.org/10.1117/1.jbo.18.12.128001
Kim HK, Kim JH, Abbas AA et al (2009) Red light of 647 nm enhances osteogenic differentiation in mesenchymal stem cells. Lasers Med Sci 24:214–222. https://doi.org/10.1007/s10103-008-0550-6
Klionsky DJ, Emr SD (1989) Membrane protein sorting: biosynthesis, transport and processing of yeast vacuolar alkaline phosphatase. EMBO J 8:2241–2250
Konno M, Hamabe A, Hasegawa S et al (2013) Adipose-derived mesenchymal stem cells and regenerative medicine. Dev Growth Differ 55:309–318. https://doi.org/10.1111/dgd.12049
Kreisler M, Christoffers AB, Willershausen B, d’Hoedt B (2003) Low-level 809 nm GaAlAs laser irradiation increases the proliferation rate of human laryngeal carcinoma cells in vitro. Lasers Med Sci 18:100–103. https://doi.org/10.1007/s10103-003-0265-7
Liu Z-J, Zhuge Y, Velazquez OC (2009) Trafficking and differentiation of mesenchymal stem cells. J Cell Biochem 106:984–991. https://doi.org/10.1002/jcb.22091
Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55–63. https://doi.org/10.1016/0022-1759(83)90303-4
Mvula B, Mathope T, Moore T, Abrahamse H (2008) The effect of low level laser irradiation on adult human adipose derived stem cells. Lasers Med Sci 23:277–282. https://doi.org/10.1007/s10103-007-0479-1
Mvula B, Moore TJ, Abrahamse H (2010) Effect of low-level laser irradiation and epidermal growth factor on adult human adipose-derived stem cells. Lasers Med Sci 25:33–39. https://doi.org/10.1007/s10103-008-0636-1
Oliveira CF, Basso FG, Lins EC et al (2010) Increased viability of odontoblast-like cells subjected to low-level laser irradiation. Laser Phys 20:1659–1666. https://doi.org/10.1134/s1054660x10130153
Ong WK, Chen HF, Tsai CT et al (2013) The activation of directional stem cell motility by green light-emitting diode irradiation. Biomaterials. https://doi.org/10.1016/j.biomaterials.2012.11.065
Peng F, Wu H, Zheng Y et al (2012) The effect of noncoherent red light irradiation on proliferation and osteogenic differentiation of bone marrow mesenchymal stem cells. Lasers Med Sci 27:645–653. https://doi.org/10.1007/s10103-011-1005-z
Polo-Corrales L, Latorre-Esteves M, Ramirez-Vick JE (2014) Scaffold design for bone regeneration. J Nanosci Nanotechnol 14:15–56. https://doi.org/10.1166/jnn.2014.9127
Renno AC, McDonnell PA, Parizotto NA et al (2007) The effects of laser irradiation on osteoblast and osteosarcoma cell proliferation and differentiation in vitro. Photomed Laser Surg 25:8–15. https://doi.org/10.1089/pho.2007.2055
Rodríguez LV, Alfonso Z, Zhang R et al (2006) Clonogenic multipotent stem cells in human adipose tissue differentiate into functional smooth muscle cells. Proc Natl Acad Sci U S A 103:12167–12172. https://doi.org/10.1073/pnas.0604850103
Soleimani M, Abbasnia E, Fathi M et al (2012) The effects of low-level laser irradiation on differentiation and proliferation of human bone marrow mesenchymal stem cells into neurons and osteoblasts—an in vitro study. Lasers Med Sci 27:423–430. https://doi.org/10.1007/s10103-011-0930-1
Tabatabaei FS, Torshabi M, Nasab MM et al (2015) Effect of low-level diode laser on proliferation and osteogenic differentiation of dental pulp stem cells. Laser Phys 25:095602. https://doi.org/10.1088/1054-660x/25/9/095602
Tani A, Chellini F, Giannelli M et al (2018) Red (635 nm), near-infrared (808 nm) and violet-blue (405 nm) photobiomodulation potentiality on human osteoblasts and mesenchymal stromal cells: a morphological and molecular in vitro study. Int J Mol Sci 19:1–23. https://doi.org/10.3390/ijms19071946
Trentz OA, Arikketh D, Sentilnathan V et al (2010) Surface proteins and osteoblast markers: characterization of human adipose tissue-derived osteogenic cells. Eur J Trauma Emerg Surg 36:457–463. https://doi.org/10.1007/s00068-010-0030-0
Tsuji W, Rubin JP, Marra KG (2014) Adipose-derived stem cells: implications in tissue regeneration. World J Stem Cells 6:312–321. https://doi.org/10.4252/wjsc.v6.i3.312
Wang Y, Huang Y-Y, Wang Y et al (2016a) Photobiomodulation of human adipose-derived stem cells using 810 nm and 980 nm lasers operates via different mechanisms of action. Biochim Biophys Acta Gen Subj. https://doi.org/10.1016/j.bbagen.2016.10.008
Wang YY, Huang YY, Wang YY et al (2016b) Photobiomodulation (blue and green light) encourages osteoblastic-differentiation of human adipose-derived stem cells: role of intracellular calcium and light-gated ion channels. Sci Rep 6:33719. https://doi.org/10.1038/srep33719
Watt FM, Driskell RR (2010) The therapeutic potential of stem cells. Philos Trans R Soc Lond B Biol Sci 365:155–163. https://doi.org/10.1098/rstb.2009.0149
Wu JY, Chen CH, Wang CZ et al (2013) Low-power laser irradiation suppresses inflammatory response of human adipose-derived stem cells by modulating intracellular cyclic AMP level and NF-κB activity. PLoS ONE 8:1–9. https://doi.org/10.1371/journal.pone.0054067
Zuk P (2013) Adipose-derived stem cells in tissue regeneration: a review. Int Sch Res Not 2013:e713959. https://doi.org/10.1155/2013/713959
Acknowledgments
This study was supported by Grant (113Z059) of the Scientific and Research Council of Turkey (TUBITAK). The cell culture experiments were performed at Bogazici University, Institute of Biomedical Engineering, Biomaterials Research Laboratory, which was supported by Bogazici University Research Fund with the Grant number 6701.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Bölükbaşı Ateş, G., Ak, A., Garipcan, B. et al. Photobiomodulation effects on osteogenic differentiation of adipose-derived stem cells. Cytotechnology 72, 247–258 (2020). https://doi.org/10.1007/s10616-020-00374-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10616-020-00374-y