Sains Malaysiana
52(7)(2023):
2069-2093
http://doi.org/10.17576/jsm-2023-5207-14
Advances in the
Bioregulation of Mesenchymal Stem Cells by Low-Level Laser Therapy during Bone
Formation: A Narrative Review
(Kemajuan dalam
Kawal Atur Sel Stem Mesenkima oleh Terapi Laser Tahap Rendah semasa
Pembentukan Tulang: Kajian Naratif)
WANG YAN PEI1,
MOHAMAD ARIF AWANG NAWI1 & NORMA AB RAHMAN2,*
1School of Dental Sciences, Universiti Sains Malaysia,
Health Campus,16150 Kubang Kerian, Kelantan, Malaysia
2Orthodontic Unit, School of Dental Sciences,
Universiti Sains Malaysia, Health Campus, 16150 Kubang Kerian, Kelantan,
Malaysia
Received: 11
November 2022/Accepted: 5 July 2023
Abstract
This article reviews the progress of research on the modulation of the
biological effects of low-level laser therapy (LLLT) on Mesenchymal stem cells
(MSC) and the influence of the basic LLLT parameters and irradiation scenarios. A thorough search of the literature
in the PubMed, Web of Science and
Embase databases, including articles
published in peer-reviewed journals, was conducted to collect relevant
information on LLLT and MSCs. A comprehensive search of PubMed, Web of Science,
and Embase databases was performed using the keywords "Low level
laser," "mesenchymal stem cells," " cell
proliferation," and "osteogenic differentiation." The search was
limited to studies published in English between 2009 and 2022, including in
vitro and in vivo studies. LLLT has the potential to
promote MSC proliferation and osteogenic differentiation, with significant
applications in bone tissue engineering. Factors that influence the biological
effects of LLLT on MSC include cell type, culture medium, duration of
irradiation, the frequency of laser irradiation, irradiation spot size, and
type of light flux distribution. The limitations of this review include
heterogeneous experimental conditions and the inability to design experiments
that consider all influencing factors simultaneously.
Keywords: Cell proliferation; low level laser; mesenchymal
stem cells; osteogenic differentiation
Abstrak
Artikel
ini mengkaji kemajuan penyelidikan mengenai modulasi kesan biologi terapi laser
peringkat rendah (LLLT) pada sel stem mesenkima (MSC) dan pengaruh parameter
LLLT asas dan senario penyinaran. Pencarian teliti kepustakaan dalam pangkalan
data PubMed, Web of Science dan Embase, termasuk artikel yang diterbitkan dalam
jurnal semakan rakan sebaya, telah dijalankan untuk mengumpul maklumat yang
berkaitan tentang LLLT dan MSC. Carian komprehensif pangkalan data PubMed, Web
of Science dan Embase telah dilakukan menggunakan kata kunci ‘laser tahap
rendah’, ‘sel stem mesenkima’, ‘percambahan sel’ dan ‘pembezaan osteogenik’.
Pencarian terhad kepada kajian yang diterbitkan dalam bahasa Inggeris antara
2009 dan 2022, termasuk kajian in vitro dan in vivo. LLLT
berpotensi untuk menggalakkan percambahan MSC dan pembezaan osteogenik dengan
aplikasi penting dalam kejuruteraan tisu tulang. Faktor yang mempengaruhi kesan
biologi LLLT pada MSC termasuk jenis sel, medium kultur, tempoh penyinaran,
kekerapan penyinaran laser, saiz tempat penyinaran dan jenis taburan fluks
cahaya. Kekangan dalam ulasan ini termasuk keadaan uji kaji heterogen dan
ketidakupayaan untuk mereka bentuk uji kaji yang mempertimbangkan semua faktor
yang mempengaruhi secara serentak.
Kata kunci: Laser tahap rendah; pembezaan osteogenik;
percambahan sel; sel stem mesenkima
REFERENCES
Ahrabi, B., Rezaei Tavirani, M., Khoramgah, M. S.,
Noroozian, M., Darabi, S., Khoshsirat, S., &
Abbaszadeh, H.A. 2019. The effect of photobiomodulation therapy on the differentiation,
proliferation, and migration of the mesenchymal stem cell: A review. Journal of
Lasers in Medical Sciences 10(Suppl.
1): S96-S103. https://doi.org/10.15171/jlms.2019.S17
Almeida-Jr., L.A., Marques, N.C.T., Prado, M.T.d.O.,
Oliveira, T.M. & Sakai, V.T. 2019. Effect of single and multiple
doses of low-level laser therapy on viability and proliferation of stem cells
from human exfoliated deciduous teeth (SHED). Lasers in Medical Science, 34(9), 1917–1924.
https://doi.org/10.1007/s10103-019-02836-y
Amaroli, A., Agas, D., Laus, F., Cuteri, V.,
Hanna, R., Sabbieti, M.G. & Benedicenti, S. 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. Frontiers in Physiology 9: 123.
https://doi.org/10.3389/fphys.2018.00123
Ballini, A., Mastrangelo,
F., Gastaldi, G., Tettamanti, L., Bukvic, N., Cantore, S., Cocco, T., Saini,
R., Desiate, A., Gherlone, E. & Scacco, S. 2015. Osteogenic differentiation
and gene expression of dental pulp stem cells under low-level laser
irradiation: A good promise for tissue engineering. J. Biol. Regul.
Homeost. Agents 29(4): 813-822. https://europepmc.org/article/med/26753641
Blatt, A., Elbaz-Greener, G.A., Tuby, H., Maltz, L.,
Siman-Tov, Y., Ben-Aharon, G., Copel, L., Eisenberg, I.,
Efrati, S., Jonas, M., Vered, Z., Tal, S., Goitein, O.
& Oron, U. 2016. Low-level laser therapy to the bone marrow reduces
scarring and improves heart function post-acute myocardial infarction in the
pig. Photomedicine
and Laser Surgery 34(11):
516-524. https://doi.org/10.1089/pho.2015.3988
Bölükbaşı Ateş, G., Ak, A., Garipcan, B.
& Gülsoy, M. 2020. Photobiomodulation effects on osteogenic
differentiation of adipose-derived stem cells. Cytotechnology 72(2): 247-258.
https://doi.org/10.1007/s10616-020-00374-y
Cardoso, M.V., do Vale Placa, R., Sant'Ana, A.C.P.,
Greghi, S.L.A., Zangrando, M.S.R., de
Rezende, M.L.R., Oliveira, R.C. & Damante, C.A. 2021.
Laser and LED photobiomodulation effects in osteogenic or regular medium on rat
calvaria osteoblasts obtained by newly forming bone technique. Lasers in Medical
Science 36(3): 541-553.
https://doi.org/10.1007/s10103-020-03056-5
Cavalcanti, M.F.X.B., Maria, D.A., de Isla, N.,
Leal-Junior, E.C.P., Joensen, J., Bjordal, J.M.,
Lopes-Martins, R.A.M.B., Diomede, F., Trubiani, O. &
Frigo, L. 2015. Evaluation of the proliferative effects induced by
low-level laser therapy in bone marrow stem cell culture. Photomedicine
and Laser Surgery 33(12):
610-616. https://doi.org/10.1089/pho.2014.3864
de Andrade, A.L.M., Luna, G.F.,
Brassolatti, P., Leite, M.N., Parisi, J.R., de Oliveira
Leal, Â.M., Frade, M.A.C., de Freitas Anibal, F. &
Parizotto, N.A. 2019. Photobiomodulation effect on the proliferation of
adipose tissue mesenchymal stem cells. Lasers in Medical Science 34(4): 677-683.
https://doi.org/10.1007/s10103-018-2642-2
de Villiers, J.A., Houreld, N.N. & Abrahamse, H.
2011. Influence of low intensity laser irradiation on isolated human adipose
derived stem cells over 72 hours and their differentiation potential into
smooth muscle cells using retinoic acid. Stem Cell Reviews and Reports 7(4): 869-882.
https://doi.org/10.1007/s12015-011-9244-8
Fageeh, H.N. 2021. Preliminary evaluation of proliferation, wound
healing properties, osteogenic and chondrogenic potential of dental pulp stem
cells obtained from healthy and periodontitis affected teeth. Cells 10(8): 2118.
https://doi.org/10.3390/cells10082118
Fallahnezhad, S., Jajarmi, V., Shahnavaz, S.,
Amini, A., Ghoreishi, S.K., Kazemi, M., Chien, S. &
Bayat, M. 2020. Improvement in viability and mineralization of
osteoporotic bone marrow mesenchymal stem cell through combined application of
photobiomodulation therapy and oxytocin. Lasers in Medical Science 35(3): 557-566.
https://doi.org/10.1007/s10103-019-02848-8
Fallahnezhad, S., Piryaei, A., Tabeie, F.,
Nazarian, H., Darbandi, H., Amini, A., Mostafavinia, A.,
Ghorishi, S.K., Jalalifirouzkouhi, A. & Bayat, M. 2016.
Low-level laser therapy with helium-neon laser improved viability of
osteoporotic bone marrow-derived mesenchymal stem cells from ovariectomy-induced
osteoporotic rats. Journal of Biomedical Optics 21(9): 98002.
https://doi.org/10.1117/1.JBO.21.9.098002
Fekrazad, R., Asefi, S., Eslaminejad, M.B.,
Taghiar, L., Bordbar, S. & Hamblin, M.R. 2019. Photobiomodulation with single and combination laser wavelengths
on bone marrow mesenchymal stem cells: Proliferation and differentiation to
bone or cartilage. Lasers in Medical Science 34(1): 115-126.
https://doi.org/10.1007/s10103-018-2620-8
Ferreira, L.S., Diniz, I.M.A., Maranduba, C.M.S.,
Miyagi, S.P.H., Rodrigues, M.F.S.D., Moura-Netto, C. &
Marques, M.M. 2019. Short-term evaluation of photobiomodulation therapy on
the proliferation and undifferentiated status of dental pulp stem cells. Lasers in
Medical Science 34(4):
659-666. https://doi.org/10.1007/s10103-018-2637-z
Gether, U. 2000. Uncovering molecular mechanisms involved in
activation of G protein-coupled receptors. Endocrine Reviews 21(1): 90-113.
https://doi.org/10.1210/edrv.21.1.0390
Han, Y., Li, X., Zhang, Y., Han, Y., Chang, F.
& Ding, J. 2019. Mesenchymal stem cells for regenerative medicine. Cells 8(8): 886.
https://doi.org/10.3390/cells8080886
Hanna, R., Agas, D., Benedicenti, S., Ferrando, S.,
Laus, F., Cuteri, V., Lacava, G., Sabbieti, M.G. &
Amaroli, A. 2019. A comparative study between the effectiveness of 980 nm photobiomodulation
delivered by hand-piece with Gaussian vs. flat-top profiles on osteoblasts
maturation. Frontiers in Endocrinology 10: 92. https://doi.org/10.3389/fendo.2019.00092
Horvát-Karajz, K., Balogh, Z., Kovács, V.,
Drrernat, A.H., Sréter, L. & Uher, F. 2009. In vitro effect of carboplatin, cytarabine, paclitaxel, vincristine, and low-power laser
irradiation on murine mesenchymal stem cells. Lasers in Surgery and Medicine 41(6): 463-469.
https://doi.org/10.1002/lsm.20791
Li, W.T., Chen, C.W. & Huang, P.Y. 2013. Effects of
low level light irradiation on the migration of mesenchymal stem cells derived
from rat bone marrow. Annual International Conference of the IEEE
Engineering in Medicine and Biology Society. IEEE Engineering in Medicine and
Biology Society. pp. 4121-4124.
https://doi.org/10.1109/EMBC.2013.6610452
Marques, M.M., Diniz, I.M.A., de
Cara, S.P.H.M., Pedroni, A.C.F., Abe, G.L.,
D'Almeida-Couto, R.S., Lima, P.L.V., Tedesco, T.K. &
Moreira, M.S. 2016. Photobiomodulation of dental derived mesenchymal stem cells: A
systematic review. Photomedicine and Laser Surgery 34(11): 500-508.
https://doi.org/10.1089/pho.2015.4038
Merigo, E., Bouvet-Gerbettaz, S., Boukhechba, F.,
Rocca, J.P., Fornaini, C. & Rochet, N. 2016. Green laser light irradiation enhances differentiation and matrix
mineralization of osteogenic cells. Journal of Photochemistry and
Photobiology. B, Biology 155: 130-136. https://doi.org/10.1016/j.jphotobiol.2015.12.005
Mester, E., Szende, B.
& Gärtner, P. 1968. The effect of laser beams on the growth of hair in mice. Radiobiologia, Radiotherapia 9(5): 621-626. https://europepmc.org/article/med/5732466
Migliario, M., Sabbatini, M., Mortellaro, C. &
Renò, F. 2018. Near infrared low-level laser therapy and cell
proliferation: The emerging role of redox sensitive signal transduction
pathways. Journal of Biophotonics 11(11):
e201800025. https://doi.org/10.1002/jbio.201800025
Min, K.H., Byun, J.H., Heo, C.Y., Kim, E.H.,
Choi, H.Y. & Pak, C.S. 2015. Effect of low-level laser therapy on
human adipose-derived stem cells: in vitro and in vivo studies. Aesthetic
Plastic Surgery 39(5):
778-782. https://doi.org/10.1007/s00266-015-0524-6
Nandy, S.B., Mohanty, S., Singh, M., Behari, M.
& Airan, B. 2014. Fibroblast growth factor-2 alone as an efficient inducer for
differentiation of human bone marrow mesenchymal stem cells into dopaminergic
neurons. Journal of Biomedical Science 21(1): 83. https://doi.org/10.1186/s12929-014-0083-1
Nurković, J., Zaletel, I., Nurković, S.,
Hajrović, Š., Mustafić, F., Isma, J.,
Škevin, A.J., Grbović, V., Filipović, M.K. &
Dolićanin, Z. 2017. Combined effects of electromagnetic field and
low-level laser increase proliferation and alter the morphology of human
adipose tissue-derived mesenchymal stem cells. Lasers in Medical Science 32(1): 151-160.
https://doi.org/10.1007/s10103-016-2097-2
Pasternak-Mnich, K., Ziemba, B., Szwed, A.,
Kopacz, K., Synder, M., Bryszewska, M. & Kujawa, J.
2019. Effect of photobiomodulation therapy on the increase of viability and
proliferation of human mesenchymal stem cells. Lasers in Surgery and Medicine 51(9): 824-833.
https://doi.org/10.1002/lsm.23107
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 in
Medical Science 27(3):
645-653. https://doi.org/10.1007/s10103-011-1005-z
Ruan, Y., Kato, H., Taguchi, Y., Yamauchi, N. &
Umeda, M. 2021. Irradiation by high-intensity red light-emitting diode
enhances human bone marrow mesenchymal stem cells osteogenic differentiation
and mineralization through Wnt/β-catenin signaling pathway. Lasers in
Medical Science 36(1):
55-65. https://doi.org/10.1007/s10103-020-03002-5
Serrage, H., Heiskanen, V., Palin, W.M., Cooper, P.R.,
Milward, M.R., Hadis, M. & Hamblin, M.R. 2019. Under the
spotlight: Mechanisms of photobiomodulation concentrating on blue and green
light. Photochemical
& Photobiological Sciences 18(8):
1877-1909. https://doi.org/10.1039/c9pp00089e
Syed-Picard, F.N., Du, Y., Lathrop, K.L.,
Mann, M.M., Funderburgh, M.L. & Funderburgh, J.L. 2015.
Dental pulp stem cells: A new cellular resource for corneal stromal
regeneration. Stem Cells Translational Medicine 4(3): 276-285. https://doi.org/10.5966/sctm.2014-0115
Tani, A., Chellini, F., Giannelli, M., Nosi, D.,
Zecchi-Orlandini, S. & Sassoli, C. 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. International Journal of Molecular Sciences 19(7): 1946.
https://doi.org/10.3390/ijms19071946
Tsai, P.J., Wang, H.S., Lin, C.H., Weng, Z.C.,
Chen, T.H. & Shyu, J.F. 2014. Intraportal injection of
insulin-producing cells generated from human bone marrow mesenchymal stem cells
decreases blood glucose level in diabetic rats. Endocrine Research 39(1): 26-33.
https://doi.org/10.3109/07435800.2013.797432
Wang, L., Wu, F., Liu, C., Song, Y., Guo, J.,
Yang, Y. & Qiu, Y. 2019. Low-level laser irradiation modulates
the proliferation and the osteogenic differentiation of bone marrow mesenchymal
stem cells under healthy and inflammatory condition. Lasers in
Medical Science 34(1):
169-178. https://doi.org/10.1007/s10103-018-2673-8
Wang, Y., Huang, Y.Y., Wang, Y., Lyu, P. &
Hamblin, M.R. 2017a. Photobiomodulation of human adipose-derived stem
cells using 810nm and 980nm lasers operates via different mechanisms of action. Biochimica Et
Biophysica Acta. General Subjects 1861(2):
441-449. https://doi.org/10.1016/j.bbagen.2016.10.008
Wang, Y., Huang, Y.Y., Wang, Y., Lyu, P. &
Hamblin, M.R. 2017b. Red (660 nm) or near-infrared (810 nm)
photobiomodulation stimulates, while blue (415 nm), green (540 nm) light
inhibits proliferation in human adipose-derived stem cells. Scientific
Reports 7(1): 7781.
https://doi.org/10.1038/s41598-017-07525-w
Wu, J.Y., Chen, C.H., Yeh, L.Y., Yeh, M.L.,
Ting, C.C. & Wang, Y.H. 2013. Low-power laser irradiation
promotes the proliferation and osteogenic differentiation of human periodontal
ligament cells via cyclic adenosine monophosphate. International Journal of Oral
Science 5(2): 85-91.
https://doi.org/10.1038/ijos.2013.38
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. Scientific
Reports 6: 37370.
https://doi.org/10.1038/srep37370
Yang, Y., Zhu, T., Wu, Y., Shu, C., Chen, Q.,
Yang, J., Luo, X. & Wang, Y. 2020. Irradiation with blue
light-emitting diode enhances osteogenic differentiation of stem cells from the
apical papilla. Lasers in Medical Science 35(9):
1981-1988. https://doi.org/10.1007/s10103-020-02995-3
Yin, K., Zhu, R., Wang, S. & Zhao, R.C. 2017.
Low-level laser effect on proliferation, migration, and antiapoptosis of
mesenchymal stem cells. Stem Cells and Development 26(10): 762-775.
https://doi.org/10.1089/scd.2016.0332
Yuan, Y., Yan, G., Gong, R., Zhang, L.,
Liu, T., Feng, C., Du, W., Wang, Y., Yang, F.,
Li, Y., Guo, S., Ding, F., Ma, W., Idiiatullina, E.,
Pavlov, V., Han, Z., Cai, B. & Yang, L. 2017. Effects of blue light emitting diode irradiation
on the proliferation, apoptosis and differentiation of bone marrow-derived
mesenchymal stem cells. Cellular Physiology and Biochemistry 43(1): 237-246.
https://doi.org/10.1159/000480344
Zare, F., Bayat, M., Aliaghaei, A. & Piryaei, A.
2020. Photobiomodulation therapy compensate the impairments of diabetic bone
marrow mesenchymal stem cells. Lasers in Medical Science 35(3): 547-556.
https://doi.org/10.1007/s10103-019-02844-y
Zare, F., Moradi, A., Fallahnezhad, S.,
Ghoreishi, S.K., Amini, A., Chien, S. & Bayat, M. 2019. Photobiomodulation with 630 plus 810 nm
wavelengths induce more in vitro cell viability of human adipose stem
cells than human bone marrow-derived stem cells. Journal of Photochemistry and
Photobiology B: Biology 201: 111658. https://doi.org/10.1016/j.jphotobiol.2019.111658
Zecha, J.A.E.M., Raber-Durlacher, J.E., Nair, R.G.,
Epstein, J.B., Sonis, S.T., Elad, S., Hamblin, M.R.,
Barasch, A., Migliorati, C.A., Milstein, D.M.J.,
Genot, M.T., Lansaat, L., van der Brink, R., Arnabat-Dominguez, J.,
van der Molen, L., Jacobi, I., van Diessen, J., de Lange, J.,
Smeele, L.E., Schubert, M.M. & Bensadoun, R.J. 2016. Low level laser therapy/photobiomodulation in the
management of side effects of chemoradiation therapy in head and neck cancer:
Part 1: Mechanisms of action, dosimetric, and safety considerations. Supportive Care in
Cancer: Official Journal of the Multinational Association of Supportive Care in
Cancer 24(6):
2781-2792. https://doi.org/10.1007/s00520-016-3152-z
Zein, R., Selting, W. & Hamblin, M.R. 2018. Review of
light parameters and photobiomodulation efficacy: Dive into complexity. Journal of
Biomedical Optics 23(12):
1-17. https://doi.org/10.1117/1.JBO.23.12.120901
Zhang, R.F., Wang, Q., Zhang, A.A., Xu, J.G.,
Zhai, L.D., Yang, X.M. & Liu, X.T. 2018. Low-level laser
irradiation promotes the differentiation of bone marrow stromal cells into
osteoblasts through the APN/Wnt/β-catenin pathway. European Review
for Medical and Pharmacological Sciences 22(9): 2860-2868. https://doi.org/10.26355/eurrev_201805_14988
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 in
Medical Science 34(7):
1473-1481. https://doi.org/10.1007/s10103-019-02750-3
Zungu, I.L., Hawkins Evans, D. & Abrahamse, H. 2009.
Mitochondrial responses of normal and injured human skin fibroblasts following
low level laser irradiation--an in vitro study. Photochemistry
and Photobiology 85(4):
987-996. https://doi.org/10.1111/j.1751-1097.2008.00523.x
*Corresponding author; email:
drnorma@usm.my
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