Enhancing the Therapeutic Potential of Mesenchymal Stem Cells with Light-Emitting Diode: Implications and Molecular Mechanisms

Mansano, Barbara Sampaio Dias Martins; da Rocha, Vitor Pocani; Antonio, Ednei Luiz; Peron, Daniele Fernanda; do Nascimento de Lima, Rafael; Tucci, Paulo Jose Ferreira; Serra, Andrey Jorge

doi:https://doi.org/10.1155/2021/6663539

Oxidative Medicine and Cellular Longevity

On this page

Abstract Introduction Materials and Methods Results Discussion Conclusion Disclosure Conflicts of Interest Acknowledgments References Copyright Related Articles

Special Issue

Insights into Photobiomodulation and Oxidative Stress: Physiological, Pathological, and Therapeutic Impact

View this Special Issue

Review Article | Open Access

Volume 2021 | Article ID 6663539 | https://doi.org/10.1155/2021/6663539

Enhancing the Therapeutic Potential of Mesenchymal Stem Cells with Light-Emitting Diode: Implications and Molecular Mechanisms

Barbara Sampaio Dias Martins Mansano,¹Vitor Pocani da Rocha,²Ednei Luiz Antonio,²Daniele Fernanda Peron,¹Rafael do Nascimento de Lima,¹Paulo Jose Ferreira Tucci,²and Andrey Jorge Serra^1,2

Academic Editor: Jayeeta Ghose

Received03 Nov 2020

Revised05 Jan 2021

Accepted22 Jan 2021

Published03 Feb 2021

Abstract

This study evaluated the effects of light-emitting diode (LED) on mesenchymal stem cells (MSCs). An electronic search was conducted in PubMed/MEDLINE, Scopus, and Web of Science database for articles published from 1980 to February 2020. Ten articles met the search criteria and were included in this review. The risk of bias was evaluated to report quality, safety, and environmental standards. MSCs were derived from adipose tissue, bone marrow, dental pulp, gingiva, and umbilical cord. Protocols for cellular irradiation used red and blue light spectrum with variations of the parameters. The LED has been shown to induce greater cellular viability, proliferation, differentiation, and secretion of growth factors. The set of information available leads to proposing a complex signaling cascade for the action of photobiomodulation, including angiogenic factors, singlet oxygen, mitogen-activated protein kinase/extracellular signal-regulated protein kinase, Janus kinase/signal transducer, and reactive oxygen species. In conclusion, although our results suggest that LED can boost MSCs, a nonuniformity in the experimental protocol, bias, and the limited number of studies reduces the power of systematic review. Further research is essential to find the optimal LED irradiation parameters to boost MSCs function and evaluate its impact in the clinical setting.

1. Introduction

Photobiomodulation (PBM) employs nonionizing forms of light sources, which encompass laser and light-emitting diode (LED) for a broad visible and infrared spectrum, and PBM-based therapy has been successfully applied in treatment of several diseases, injuries, and disorders [1]. Acquaintance with the mechanisms subjacent the effects of PBM has been of considerable interest, and a well-accepted view is that the light energy delivered to tissues is absorbed by the cell chromophores, favouring the production of adenosine triphosphate (ATP) [2, 3]. Nevertheless, beneficial effects on inflammation, oxidative stress, survival, and the regeneration of tissues have been reported by several researchers [4–7].

Concerning LED, when the first one was developed in 1998 by Harry Whelan and his group at the NASA space medicine laboratory [8], this technology had some characteristics that diverge them from laser devices. While LED are noncoherent and quasimonochromatic light sources [9] based on the phenomenon of electroluminescence of semiconductor materials [10], laser emits, in a stimulated manner, a monochromatic, and coherent light beam of low divergence [11]. Besides that, it is important to quote that those different properties would still photoactivate cells without causing heat changes or damage. Notwithstanding, benefits are perceptible in LED when compared to lasers, such as increased safety and durability, lower cost, ease of use, and more flexibility in the irradiated area size [11, 12], although the biological effects of light on irradiated cells are similar in both laser and LED [13, 14]. LED phototherapy has either been well-proven to have an effective benefit in a wide variety of clinical indications such as pain relief, skin injuries, rheumatological diseases, muscle disorders, and infections, suggesting as well that LED might have a powerful role to play in the clinical practice for a variety of conditions. [7, 15–27].

The LED has also emerged to have important effects on mesenchymal stem cells (MSCs) [28], easily cultivated multipotent stem cells which can be isolated from various adult tissues, therefore opening a new window for PBM application into strategies being currently pursued to improve therapy with MSCs. Among the advantages of MSCs usage, it is possible to observe the availability in ubiquitous sources, the extensive ability of proliferation and multilineage differentiation, easy isolation, low immunogenicity, and paracrine potential [29, 30]. In addition, it is important to cite the immunomodulatory proprieties of MSCs, which could be used in the treatment of many disorders like promoting maintenance of the ratio of Treg and T helper cells in systemic lupus erythematosus [31], and the proosteogenic capacity, mainly presented in oral tissue MSCs [31, 32].

MSCs reside in a complex microenvironment among other cell types and biochemical stimuli, which influence if the cell will differentiate or self-renew. Mechanical factors are also being recognized as regulators. Therefore, the microenvironment is significantly an influencer of the role and differentiation of MSCs through biochemical, biomechanical, and biophysical factors [33].

Although being a promising therapy, mostly to the poor engrafting of implanted cells, low survival rates are common for long periods and MSC therapy has generated unsatisfactory results in numerous clinical conditions [34, 35]. Hence, since LED was referred to have the biological effects mentioned above, it could be applied to overcome the current limitations of MSC therapy more easily. Thereby, preconditioning of MSCs with LEDs before transplantation may be a usual procedure to improve tissue engineering and cell therapy in the future [36, 37].

To the best of our knowledge, most of the articles evaluated the repercussion of PBM on MSCs, as illustrated in different systematic reviews [28, 38–40], and the MSC response to LED irradiation remains unclear. Therefore, based on the plethora of biology actions that make the MSCs promising to regenerative medicine [29] and the possible cytoprotective effect of the PBM, we aimed this systematic review to summarize the current evidence about the effects of LED in mesenchymal stem cells (MSCs) and to identify the underlying mechanisms found to underpin this effect.

2. Materials and Methods

2.1. Search Strategy

The study was carried out according to PRISMA guidelines (Figure 1). The search for published articles into the effect of LEDs on MSCs was conducted in PubMed, Scopus, and Web of Science databases. The articles retrieved were limited to the English language and were for the period from January 1980 to February 2020. The MeSH terms and Scopus international data lines were used to find keywords related to “photobiomodulation,” “phototherapy,” “light-emitting diode,” “stem cells,” and “mesenchymal stem cells.” MeSH terms were used individually or combined to increase the findings. Data extraction involved MSC experimental methodology, LED parameters, and results. Duplicate articles from the database search results were removed.

2.2. Study Selection

Screening for potentially eligible studies was examined by considering the title and abstracts close to the keywords regarding the theme. Additionally, two independent reviewers applied predetermined inclusion criteria to full studies. Conflicts were solved by a third independent researcher. Articles investigating in vitro procedural or methodological applications of LED were accepted. The application of the irradiation could be to any plate or culture bottle. At the end of the selection process, after reading the full texts, articles that matched inclusion criteria are included: a quantitative or semi-quantitative measure; English language; LED irradiation provided as an intervention to at least one of the treatment groups; MSCs experimentally analyzed; to report a minimum of LED parameters; or the missing parameter had to be calculable using alternate parameters. The exclusion criteria were as follows: established cell lines; missing LED parameters or not possible to calculate; papers not published in the English language; phototherapy not using LED; and review articles with or without meta-analysis. Figure 1 shows the process of study selection.

2.3. Risk of Bias

Potentially eligible articles were printed, reviewed, and critically judged by three independent reviewers. Bias is a reliable method to assess quality, safety, and environmental standards of clinical and experimental studies [41]; therefore, the studies were analyzed using an adapted version for cellular research [42]. Risk of bias included selection (systematic differences in the comparison groups), performance (systematic differences introduced during the study), detection (systematic differences in the outcome assessment between groups), attrition (systematic differences in excluding study units between groups), reporting (systematic omission of results in the study documentation/publication), confounding (systematic differences in factors potentially influencing the results between groups), appropriate statistical methods, and other bias.

3. Results

3.1. Study Selection

Figure 1 shows a flowchart of the search, conducted using the three databases. Overall, 1933 articles were found in an early screening. From the initial potentially relevant articles identified, 1880 were excluded because they did not meet the inclusion criteria as follows: no LED irradiation (); systematic reviews (); established cell lines (); no English language (); and congress abstracts (). After this, 53 articles remained, and they were fully examined to check closely the exclusion criteria. Then, 27 repeated studies were excluded as well as 16 other papers with lost or impossible to calculate LED parameters. Finally, 10 articles served as the basis for this systematic review.

3.2. Risk of Bias

Figure 2(a) illustrates the risk of bias evaluated for each included study. Firstly, articles were surveyed for the presence or absence of key sections: 40% did not mention ethical statement and 10% did not give a description of measurement precision and variability. Then, low and high risk of bias was judged as illustrated in Figure 2(b), in which the categories that presented more studies (i.e., 100%) in low risk were as follows: other bias; appropriate statistical methods; confounding bias; reporting bias; and selection bias—“allocation concealment” and “appropriate control group selection.” Some categories expressed 100% concerning high risk: detection and performance bias. Selection bias (“randomization”) was 60% at high risk.

(a)

(b)

3.3. Interventions

Table 1 describes in detail the methodology of MSCs used in seven articles. MSCs were derived from two animal species (60% human, 40% rodents) and several sources (30% bone marrow, 30% umbilical cord, 20% tooth pulp, 10% adipocyte, and 10% gingiva). Cell concentration and passages had high variance. One study did not specify the rodent strain used for obtaining MSCs, and three papers did not report the cellular passage. Five studies did not report donor genders. Table 2 shows the LED parameters used in the articles. Studies showed a huge variety of irradiating primary MSCs using LEDs. Wavelengths were mostly within the red spectrum, ranging from 620 to 800 nm. One study considered irradiating cells at the blue wavelength (400 to 480 nm and another paper has applied irradiations in a broad spectrum of light, ranging from 400 to 800 nm). Many studies have not reported dimensions for flasks, dishes, or culture wells. In this regard, approximate growth surface areas were considered in the basic dimension guide (e.g., https://www.corning.com/catalog/cls/documents/application-notes/CLS-AN-209.pdf): 96-well plate (0.32 cm²); 24-well plate (1.9 cm²); 35 mm or 3.5 cm plate (9 cm²); and T75 bottles (75 cm²). Thus, the irradiance area varied from 0.32 to 75 cm². Potency reached 0.848 to 900 mW, whereas the irradiance varied from 1.65 to 100 mW/cm², appearing differently when distinct authors. Energy varied from 0.102 to 450 J, and radiant exposure reached 0.075 to 32 J/cm². Irradiation time reported reached 10 to 3636 seconds, appearing differently when distinct authors. Single irradiation was most used, and the timeline varied between 1 and 28 days.

The main results are presented in Table 3. Most studies that assessed viability, proliferation, and differentiation showed that the cells responded positively to LED. These findings were accompanied by the increased metabolic potential of the cells, as illustrated by higher ATP content and mitochondrial activity. MSCs irradiated with red LED also had an increased secretion of nitric oxide (NO) and growth factors, such as the fibroblast growth factor (FGF), hepatocyte growth factor (HGF), and vascular endothelial growth factor (VEGF). There was no effect of LED on scratch, with one study reporting increased levels of genetic self-renewal markers. Only one study has reported an adverse effect of LED to increased DNA fragmentation. Moreover, the only study that has used blue wavelengths reported decreased viability using 3-(4,5-dimethyl-2-thiazolyl)-2,5-diphenyl-2H-tetrazolium bromide assay.

4. Discussion

Most of the therapeutic effects of MSCs are unsatisfactory because implanted cells have low engrafting and do not survive for a long time. In light of these undesirables, genetic approaches were used to improve survival, engraftment, proliferation, and differentiation of MSCs [43]. MSC preconditioning has been another strategy to enhance functionally and cellular resistance into the hostile tissue [43]. In this setting, the present study was carried out to systematically review the literature on the effectiveness of LED in optimizing the therapeutic potential of MSCs.

In respect to the irradiation approach, most studies have applied LED in the red band, varying between 620 and 800 nm [13, 44–51]. The red light was chosen because it has been well-reported to rise the proliferation rate of various MSCs lines [44, 45, 52]. Besides, the majority of LED applications on MSCs were performed with irradiances of up to 15 mW/cm² and radiant exposure ranging from 0.075 to 4 J/cm² [13, 44–47, 50, 51]. This LED exposure programming is very helpful to enhance cell proliferation [13, 44, 47, 53], showing to be in line with the findings described in Table 3. MSC proliferation was positively influenced by LED as analyzed by different assays. On the other hand, the only study that used LEDs at 420-480 nm wavelength reported a lower rate of proliferation compared to non-irradiated MSCs over the 28-day follow-up [54], indicating that blue light does not seem subtle to enhance MSCs.

The greatest cell proliferation was accompanied by a range of up-regulated cellular responses by red-light, including clonogenic potential [44, 51], osteogenic differentiation [44], gametogenesis [50], and endothelial as well as epithelial cell formation [46]. Only one study has reported that LED can induce negative effects as determined by MTT assay [54] and DNA fragmentation [48]. This may be a result of the high irradiance applied to the cells, which was much higher than most studies included in the review that has applied red-light. High irradiance has also been used by Lipovsky et al. [49] with increased cell proliferation; however, the authors have not examined any apoptosis marker. Finally, the number of irradiations varies between different studies (see Table 2). The better frequency of irradiations affecting MSCs has not yet been determined; however, there are data reporting that LED effect on the proliferation by single-dose irradiation is temporary, and multiple stimuli are necessary for the optimization of MSC growth [44, 55].

Biological mechanisms of light therapy are not yet fully understood, and many of the data come from investigations of low-level laser role on MSCs [56, 57]. It is difficult to assume a directly comparable effect of laser with LED because these light sources have some different features. Notwithstanding, in recent years, it has become that LED performs equally to medical lasers [58], with a suitable alternative without the laser’s disadvantages such as heat production, narrow beam width, and high charges [59]. Mitochondrial respiratory chain activation is a well-described mechanism of red-light to increase ATP production which may accelerate mitosis [44, 60–62], and three studies in this review have reported increased proliferation associated with higher ATP level and mitochondrial activity [44, 45, 51]. The set of information available leads to proposing a complex signaling cascade, including singlet oxygen, mitogen-activated protein kinase/extracellular signal-regulated protein kinase, Janus kinase/signal transducer, and reactive oxygen species [44, 63–67].

In this review, two studies have reported a significant increase in VEGF, FGF, HGF, and NO content, respectively [45, 46, 49, 51]. These paracrine effects and immune regulatory functions of MSCs have been used to successfully treat a variety of tissue injury-related diseases [68, 69]. Moreover, the stimulation of angiogenesis is a very important effect of red-light to increase proliferation capacity [70, 71]. Thus, Szymanska et al. [72] reported an increased endothelial cell proliferation after light stimulation as possibly mediated by VEGF.

Therefore, the red LED may be associated with a prosurvival signal in the MSCs that added to the increased production of ATP and growth factor secretion would lead to greater cellular response to proliferation and differentiation. We summarize this network of red LED irradiation in Figure 3.

Although LED therapy could bring benefits in MSCs engineering, there was no unanimity regarding the source, nor the quantity and passage used in the experiments. Moreover, quality guideline criteria revealed that many of the included manuscripts had a high risk for detection, performance, and selection bias. These bias categories may be associated with problems in adhering to the study protocol, systematic differences introduced during the study, and lack of blinding results to study group or exposure level [42]. It is intended that a high risk of bias can potentially compromise the confidentiality of studies and influence the translation of findings in vitro to experiments using animals or clinical trials in the future.

Furthermore, after analyzing the studies in this review, it is important to quote some perspectives and limitations. The lack of studies available in irradiating MSCs with LEDs such as in vitro studies that mimic a hostile microenvironment, commonly found in transplantation sites, as well as in vivo experimentation and clinical trials possibly hindered the definition of a more effective irradiation protocol. Besides that, the lack of dosimetric parameters in studies that were not included in this review impossibilities the reproducibility and replicability of the results by other authors, also hindering determining the best parameter of irradiation.

5. Conclusion

Although the small number of studies limits the power of systematic review on photobiomodulation, evidence was found to suggest that red LED with a radiant exposure up to 7.2 J/cm², which can be an effective approach to boost MSC therapy. Overall, MSCs exposed to LED have shown enhanced viability, proliferation, differentiation, cell metabolism, and secretion of angiogenic factors compared to nonirradiated MSCs.

Disclosure

Funding sources were not involved in the study design, collection, analysis, or interpretation of data. The content is solely the responsibility of the authors and does not necessarily represent the official views of the funding sources.

Conflicts of Interest

The authors declare that they have no conflict of interest.

Acknowledgments

This work was supported by the São Paulo Research Foundation (FAPESP) (grant 2018/06865-7) and Brazilian National Council for Scientific and Technological Development (CNPq) (grant 305527/2017-7).

References

S. R. Tsai and M. R. Hamblin, “Biological effects and medical applications of infrared radiation,” Journal of Photochemistry and Photobiology. B, vol. 170, pp. 197–207, 2017.
View at: Publisher Site | Google Scholar
F. Ginani, D. M. Soares, M. P. . V. Barreto, and C. A. G. Barboza, “Effect of low-level laser therapy on mesenchymal stem cell proliferation: a systematic review,” Lasers in Medical Science, vol. 30, no. 8, pp. 2189–2194, 2015.
View at: Publisher Site | Google Scholar
Y. Wang, Y. Y. Huang, Y. Wang, P. Lyu, and M. R. Hamblin, “Photobiomodulation (blue and green light) encourages osteoblastic- differentiation of human adipose-derived stem cells: role of intracellular calcium and light-gated ion channels,” Scientific Reports, vol. 6, no. 1, article 33719, 2016.
View at: Publisher Site | Google Scholar
H. A. de Oliveira, E. L. Antonio, G. Arsa et al., “Photobiomodulation leads to reduced oxidative stress in rats submitted to high-intensity resistive exercise,” Oxidative Medicine and Cellular Longevity, vol. 2018, Article ID 5763256, 9 pages, 2018.
View at: Publisher Site | Google Scholar
M. T. Manchini, A. J. Serra, R. . S. Feliciano et al., “Amelioration of cardiac function and activation of anti-inflammatory vasoactive peptides expression in the rat myocardium by low level laser therapy,” PLoS One, vol. 9, no. 7, article e101270, 2014.
View at: Publisher Site | Google Scholar
M. P. O. Rosso, D. Buchaim, N. Kawano, G. Furlanette, K. Pomini, and R. Buchaim, “Photobiomodulation therapy (PBMT) in peripheral nerve regeneration: a systematic review,” Bioengineering, vol. 5, no. 2, p. 44, 2018.
View at: Publisher Site | Google Scholar
T. G. Stancker, S. S. Vieira, A. J. Serra et al., “Can photobiomodulation associated with implantation of mesenchymal adipose-derived stem cells attenuate the expression of MMPs and decrease degradation of type II collagen in an experimental model of osteoarthritis?” Lasers in Medical Science, vol. 33, no. 5, pp. 1073–1084, 2018.
View at: Publisher Site | Google Scholar
H. T. Whelan, E. V. Buchmann, A. Dhokalia et al., “Effect of NASA light-emitting diode irradiation on molecular changes for wound healing in diabetic mice,” Journal of Clinical Laser Medicine & Surgery, vol. 21, no. 2, pp. 67–74, 2003.
View at: Publisher Site | Google Scholar
H. T. Whelan, R. L. Smits Jr., E. V. Buchman et al., “Effect of NASA light-emitting diode irradiation on wound healing,” Journal of Clinical Laser Medicine & Surgery, vol. 19, no. 6, pp. 305–314, 2001.
View at: Publisher Site | Google Scholar
K. F. Renk, Basics of Laser Physics, Springer, 2012.
View at: Publisher Site
V. Heiskanen and M. R. Hamblin, “Photobiomodulation: lasers vs. light emitting diodes?” Photochemical & Photobiological Sciences, vol. 17, no. 8, pp. 1003–1017, 2018.
View at: Publisher Site | Google Scholar
S. Y. Tam, V. C. W. Tam, S. Ramkumar, M. L. Khaw, H. K. W. Law, and S. W. Y. Lee, “Review on the cellular mechanisms of low-level laser therapy use in oncology,” Frontiers in Oncology, vol. 10, p. 1255, 2020.
View at: Publisher Site | Google Scholar
F. Peng, H. Wu, Y. Zheng, X. Xu, and J. Yu, “The effect of noncoherent red light irradiation on proliferation and osteogenic differentiation of bone marrow mesenchymal stem cells,” Lasers in Medical Science, vol. 27, no. 3, pp. 645–653, 2012.
View at: Publisher Site | Google Scholar
Y. Ruan, H. Kato, Y. Taguchi, N. Yamauchi, and M. Umeda, “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, vol. 36, no. 1, pp. 55–65, 2021.
View at: Publisher Site | Google Scholar
R. G. Calderhead, W. S. Kim, T. Ohshiro, M. A. Trelles, and D. Vasily, “Adjunctive 830 nm light-emitting diode therapy can improve the results following aesthetic procedures,” Laser Therapy, vol. 24, no. 4, pp. 277–289, 2015.
View at: Publisher Site | Google Scholar
N. G. Yeh, C.-H. Wu, and T. C. Cheng, “Light-emitting diodes—their potential in biomedical applications,” Renewable and Sustainable Energy Reviews, vol. 14, no. 8, pp. 2161–2166, 2010.
View at: Publisher Site | Google Scholar
W. S. Kim and R. G. Calderhead, “Is light-emitting diode phototherapy (LED-LLLT) really effective?” Laser Therapy, vol. 20, no. 3, pp. 205–215, 2011.
View at: Publisher Site | Google Scholar
R. Serhal, N. Saliba, G. Hilal et al., “Effect of adipose-derived mesenchymal stem cells on hepatocellular carcinoma:In vitroinhibition of carcinogenesis,” World Journal of Gastroenterology, vol. 25, no. 5, pp. 567–583, 2019.
View at: Publisher Site | Google Scholar
W. Jing, Y. Chen, L. Lu et al., “Human umbilical cord blood-derived mesenchymal stem cells producing IL15 eradicate established pancreatic tumor in syngeneic mice,” Molecular Cancer Therapeutics, vol. 13, no. 8, pp. 2127–2137, 2014.
View at: Publisher Site | Google Scholar
T. C. Kao, H. H. C. Lee, A. Higuchi et al., “Suppression of cancer-initiating cells and selection of adipose-derived stem cells cultured on biomaterials having specific nanosegments,” Journal of Biomedical Materials Research. Part B, Applied Biomaterials, vol. 102, no. 3, pp. 463–476, 2014.
View at: Publisher Site | Google Scholar
E. S. Iplik, B. Ertugrul, I. Kozanoglu, Y. Baran, and B. Cakmakoglu, “An answer to colon cancer treatment by mesenchymal stem cell originated from adipose tissue,” Iranian Journal of Basic Medical Sciences, vol. 21, no. 5, pp. 465–468, 2018.
View at: Publisher Site | Google Scholar
Y. Yuan, C. Zhou, X. Chen, C. Tao, H. Cheng, and X. Lu, “Suppression of tumor cell proliferation and migration by human umbilical cord mesenchymal stem cells: a possible role for apoptosis and Wnt signaling,” Oncology Letters, vol. 15, no. 6, pp. 8536–8544, 2018.
View at: Publisher Site | Google Scholar
S. Bruno, F. Collino, M. C. Deregibus, C. Grange, C. Tetta, and G. Camussi, “Microvesicles derived from human bone marrow mesenchymal stem cells inhibit tumor growth,” Stem Cells and Development, vol. 22, no. 5, pp. 758–771, 2013.
View at: Publisher Site | Google Scholar
A. E. Shafei, M. A. Ali, H. G. Ghanem et al., “Mesenchymal stem cell therapy: A promising cell-based therapy for treatment of myocardial infarction,” The Journal of Gene Medicine, vol. 19, no. 12, 2017.
View at: Publisher Site | Google Scholar
A. Karamini, A. Bakopoulou, D. Andreadis, K. Gkiouras, and A. Kritis, “Therapeutic potential of mesenchymal stromal stem cells in rheumatoid arthritis: a systematic review of in vivo studies,” Stem Cell Reviews and Reports, vol. 16, no. 2, pp. 276–287, 2020.
View at: Publisher Site | Google Scholar
Y. Chen, J. Shen, K. Ke, and X. Gu, “Clinical potential and current progress of mesenchymal stem cells for Parkinson's disease: a systematic review,” Neurological Sciences, vol. 41, no. 5, pp. 1051–1061, 2020.
View at: Publisher Site | Google Scholar
J. AdiwinataPawitan, “Exploring the most promising stem cell therapy in liver failure: a systematic review,” Stem Cells International, vol. 2019, Article ID 2782548, 15 pages, 2019.
View at: Publisher Site | Google Scholar
M. M. Marques, I. M. A. Diniz, S. P. H. M. de Cara et al., “Photobiomodulation of dental derived mesenchymal stem cells: a systematic review,” Photomedicine and Laser Surgery, vol. 34, no. 11, pp. 500–508, 2016.
View at: Publisher Site | Google Scholar
W. Tsuji, J. P. Rubin, and K. G. Marra, “Adipose-derived stem cells: implications in tissue regeneration,” World J Stem Cells, vol. 6, no. 3, pp. 312–321, 2014.
View at: Publisher Site | Google Scholar
A. Rühle, R. Lopez Perez, B. Zou, A. L. Grosu, P. E. Huber, and N. H. Nicolay, “The therapeutic potential of mesenchymal stromal cells in the treatment of chemotherapy-induced tissue damage,” Stem Cell Reviews and Reports, vol. 15, no. 3, pp. 356–373, 2019.
View at: Publisher Site | Google Scholar
G. Spagnuolo, B. Codispoti, M. Marrelli, C. Rengo, S. Rengo, and M. Tatullo, “Commitment of oral-derived stem cells in dental and maxillofacial applications,” Dentistry Journal, vol. 6, no. 4, p. 72, 2018.
View at: Publisher Site | Google Scholar
A. Ballini, S. Cantore, S. Scacco, D. Coletti, and M. Tatullo, “Mesenchymal stem cells as promoters, enhancers, and playmakers of the translational regenerative medicine 2018,” Stem Cells International, vol. 2018, 2018.
View at: Publisher Site | Google Scholar
M. Marrelli, B. Codispoti, R. M. Shelton et al., “Dental pulp stem cell mechanoresponsiveness: effects of mechanical stimuli on dental pulp stem cell behavior,” Frontiers in Physiology, vol. 9, 2018.
View at: Publisher Site | Google Scholar
E. Samper, A. Diez-Juan, J. A. Montero, and P. Sepúlveda, “Cardiac cell therapy: boosting mesenchymal stem cells effects,” Stem Cell Reviews and Reports, vol. 9, no. 3, pp. 266–280, 2013.
View at: Publisher Site | Google Scholar
J. Y. Wu, C. H. Chen, C. Z. Wang, M. L. Ho, M. L. Yeh, and Y. H. Wang, “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, vol. 8, no. 1, article e54067, 2013.
View at: Publisher Site | Google Scholar
L. Wang, F. Wu, C. Liu et al., “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, vol. 34, no. 1, pp. 169–178, 2019.
View at: Publisher Site | Google Scholar
A. Castilho-Fernandes, T. G. Lopes, F. U. Ferreira et al., “Adipogenic differentiation of murine bone marrow mesenchymal stem cells induced by visible light via photo- induced biomodulation,” Photodiagnosis and Photodynamic Therapy, vol. 25, pp. 119–127, 2019.
View at: Publisher Site | Google Scholar
M. Bayat, A. Virdi, F. Rezaei, and S. Chien, “Comparison of the in vitro effects of low-level laser therapy and low-intensity pulsed ultrasound therapy on bony cells and stem cells,” Progress in Biophysics and Molecular Biology, vol. 133, pp. 36–48, 2018.
View at: Publisher Site | Google Scholar
R. Fekrazad, S. Asefi, M. Allahdadi, and K. A. M. Kalhori, “Effect of photobiomodulation on mesenchymal stem cells,” Photomedicine and Laser Surgery, vol. 34, no. 11, pp. 533–542, 2016.
View at: Publisher Site | Google Scholar
B. Ahrabi, M. Rezaei Tavirani, M. S. Khoramgah et al., “The effect of photobiomodulation therapy on the differentiation, proliferation, and migration of the mesenchymal stem cell: a review,” J Lasers Med Sci, vol. 10, no. 5, pp. S96–s103, 2019.
View at: Publisher Site | Google Scholar
J. A. C. Sterne, J. Savović, M. J. Page et al., “RoB 2: a revised tool for assessing risk of bias in randomised trials,” BMJ, vol. 366, p. l4898, 2019.
View at: Google Scholar
G. O. Samuel, S. Hoffmann, R. A. Wright et al., “Guidance on assessing the methodological and reporting quality of toxicologically relevant studies: a scoping review,” Environment International, vol. 92-93, pp. 630–646, 2016.
View at: Publisher Site | Google Scholar
A. A. Karpov, D. V. Udalova, M. G. Pliss, and M. M. Galagudza, “Can the outcomes of mesenchymal stem cell-based therapy for myocardial infarction be improved? Providing weapons and armour to cells,” Cell Proliferation, vol. 50, no. 2, p. e12316, 2017.
View at: Publisher Site | Google Scholar
W. T. Li, Y. C. Leu, and J. L. Wu, “Red-light light-emitting diode irradiation increases the proliferation and osteogenic differentiation of rat bone marrow mesenchymal stem cells,” Photomedicine and Laser Surgery, vol. 28, Suppl 1, pp. S-157–S-165, 2010.
View at: Publisher Site | Google Scholar
M. J. Holder, M. R. Milward, W. M. Palin, M. A. Hadis, and P. R. Cooper, “Effects of red light-emitting diode irradiation on dental pulp cells,” Journal of Dental Research, vol. 91, no. 10, pp. 961–966, 2012.
View at: Publisher Site | Google Scholar
I. S. Park, P. S. Chung, J. C. Ahn, and A. Leproux, “Human adipose-derived stem cell spheroid treated with photobiomodulation irradiation accelerates tissue regeneration in mouse model of skin flap ischemia,” Lasers in Medical Science, vol. 32, no. 8, pp. 1737–1746, 2017.
View at: Publisher Site | Google Scholar
A. Babaee, S. N. Nematollahi-mahani, M. Shojaei, S. Dehghani-Soltani, and M. Ezzatabadipour, “Effects of polarized and non-polarized red-light irradiation on proliferation of human Wharton's jelly-derived mesenchymal cells,” Biochemical and Biophysical Research Communications, vol. 504, no. 4, pp. 871–877, 2018.
View at: Publisher Site | Google Scholar
K. L. D. Vale, D. A. Maria, L. C. Picoli et al., “The effects of photobiomodulation delivered by light-emitting diode on stem cells from human exfoliated deciduous teeth: a study on the relevance to pluripotent stem cell viability and proliferation,” Photomedicine and Laser Surgery, vol. 35, no. 12, pp. 659–665, 2017.
View at: Publisher Site | Google Scholar
A. Lipovsky, U. Oron, A. Gedanken, and R. Lubart, “Low-level visible light (LLVL) irradiation promotes proliferation of mesenchymal stem cells,” Lasers in Medical Science, vol. 28, no. 4, pp. 1113–1117, 2013.
View at: Publisher Site | Google Scholar
A. Babaee, S. N. Nematollahi-Mahani, S. Dehghani-Soltani, M. Shojaei, and M. Ezzatabadipour, “Photobiomodulation and gametogenic potential of human Wharton's jelly-derived mesenchymal cells,” Biochemical and Biophysical Research Communications, vol. 514, no. 1, pp. 239–245, 2019.
View at: Publisher Site | Google Scholar
K. Kim, J. Lee, H. Jang et al., “Photobiomodulation enhances the angiogenic effect of mesenchymal stem cells to mitigate radiation-induced enteropathy,” International Journal of Molecular Sciences, vol. 20, no. 5, p. 1131, 2019.
View at: Publisher Site | Google Scholar
Y. Yuan, G. Yan, R. Gong et al., “Effects of blue light emitting diode irradiation on the proliferation, apoptosis and differentiation of bone marrow-derived mesenchymal stem cells,” Cellular Physiology and Biochemistry, vol. 43, no. 1, pp. 237–246, 2017.
View at: Publisher Site | Google Scholar
S. Dehghani Soltani, A. Babaee, M. Shojaei et al., “Different effects of energy dependent irradiation of red and green lights on proliferation of human umbilical cord matrix-derived mesenchymal cells,” Lasers in Medical Science, vol. 31, no. 2, pp. 255–261, 2016.
View at: Publisher Site | Google Scholar
T. Zhu, Y. Wu, X. Zhou, Y. Yang, and Y. Wang, “Irradiation by blue light-emitting diode enhances osteogenic differentiation in gingival mesenchymal stem cells in vitro,” Lasers in Medical Science, vol. 34, no. 7, pp. 1473–1481, 2019.
View at: Publisher Site | Google Scholar
W. T. Li and Y. C. Leu, “Effects of low level red-light irradiation on the proliferation of mesenchymal stem cells derived from rat bone marrow,” Annu Int Conf IEEE Eng Med Biol Soc, vol. 2007, pp. 5830–5833, 2007.
View at: Publisher Site | Google Scholar
B. Mvula, T. J. Moore, and H. Abrahamse, “Effect of low-level laser irradiation and epidermal growth factor on adult human adipose-derived stem cells,” Lasers in Medical Science, vol. 25, no. 1, pp. 33–39, 2010.
View at: Publisher Site | Google Scholar
H. Tuby, L. Maltz, and U. Oron, “Low-level laser irradiation (LLLI) promotes proliferation of mesenchymal and cardiac stem cells in culture,” Lasers in Surgery and Medicine, vol. 39, no. 4, pp. 373–378, 2007.
View at: Publisher Site | Google Scholar
M. R. Hamblin, “Mechanisms and mitochondrial redox signaling in photobiomodulation,” Photochemistry and Photobiology, vol. 94, no. 2, pp. 199–212, 2018.
View at: Publisher Site | Google Scholar
E. Priglinger, J. Maier, S. Chaudary et al., “Photobiomodulation of freshly isolated human adipose tissue-derived stromal vascular fraction cells by pulsed light-emitting diodes for direct clinical application,” Journal of Tissue Engineering and Regenerative Medicine, vol. 12, no. 6, pp. 1352–1362, 2018.
View at: Publisher Site | Google Scholar
A. Ekizer, T. Uysal, E. Güray, and Y. Yüksel, “Light-emitting diode photobiomodulation: effect on bone formation in orthopedically expanded suture in rats--early bone changes,” Lasers in Medical Science, vol. 28, no. 5, pp. 1263–1270, 2013.
View at: Publisher Site | Google Scholar
J. T. Eells, M. T. Wong-Riley, J. VerHoeve et al., “Mitochondrial signal transduction in accelerated wound and retinal healing by near-infrared light therapy,” Mitochondrion, vol. 4, no. 5-6, pp. 559–567, 2004.
View at: Publisher Site | Google Scholar
A. Mamalis, D. Siegel, and J. Jagdeo, “Visible red light emitting diode photobiomodulation for skin fibrosis: key molecular pathways,” Curr Dermatol Rep, vol. 5, no. 2, pp. 121–128, 2016.
View at: Publisher Site | Google Scholar
M. A. Dall Agnol, R. A. Nicolau, C. J. de Lima, and E. Munin, “Comparative analysis of coherent light action (laser) versus non-coherent light (light-emitting diode) for tissue repair in diabetic rats,” Lasers in Medical Science, vol. 24, no. 6, pp. 909–916, 2009.
View at: Publisher Site | Google Scholar
X. Gao and D. Xing, “Molecular mechanisms of cell proliferation induced by low power laser irradiation,” Journal of Biomedical Science, vol. 16, no. 1, p. 4, 2009.
View at: Publisher Site | Google Scholar
S. W. Jere, N. N. Houreld, and H. Abrahamse, “Photobiomodulation at 660 nm stimulates proliferation and migration of diabetic wounded cells via the expression of epidermal growth factor and the JAK/STAT pathway,” Journal of Photochemistry and Photobiology. B, vol. 179, pp. 74–83, 2018.
View at: Publisher Site | Google Scholar
J. E. Kim, Y. J. Woo, K. M. Sohn, K. H. Jeong, and H. Kang, “Wnt/β-catenin and ERK pathway activation: a possible mechanism of photobiomodulation therapy with light-emitting diodes that regulate the proliferation of human outer root sheath cells,” Lasers in Surgery and Medicine, vol. 49, no. 10, pp. 940–947, 2017.
View at: Publisher Site | Google Scholar
Y. H. Rhee, J. H. Moon, J. Y. Jung, C. Oh, J. C. Ahn, and P. S. Chung, “Effect of photobiomodulation therapy on neuronal injuries by ouabain: the regulation of Na, K-ATPase; Src; and mitogen-activated protein kinase signaling pathway,” BMC Neuroscience, vol. 20, no. 1, p. 19, 2019.
View at: Publisher Site | Google Scholar
S. Maacha, H. Sidahmed, S. Jacob et al., “Paracrine mechanisms of mesenchymal stromal cells in angiogenesis,” Stem Cells International, vol. 2020, Article ID 4356359, 12 pages, 2020.
View at: Publisher Site | Google Scholar
X. L. Fan, Y. Zhang, X. Li, and Q. L. Fu, “Mechanisms underlying the protective effects of mesenchymal stem cell-based therapy,” Cellular and Molecular Life Sciences, vol. 77, no. 14, pp. 2771–2794, 2020.
View at: Publisher Site | Google Scholar
T. S. de Oliveira, A. J. Serra, M. T. Manchini et al., “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 in Medical Science, vol. 30, no. 1, pp. 217–223, 2015.
View at: Publisher Site | Google Scholar
H. Tuby, L. Maltz, and U. Oron, “Modulations of VEGF and iNOS in the rat heart by low level laser therapy are associated with cardioprotection and enhanced angiogenesis,” Lasers in Surgery and Medicine, vol. 38, no. 7, pp. 682–688, 2006.
View at: Publisher Site | Google Scholar
J. Szymanska, K. Goralczyk, J. J. Klawe et al., “Phototherapy with low-level laser influences the proliferation of endothelial cells and vascular endothelial growth factor and transforming growth factor-beta secretion,” Journal of Physiology and Pharmacology, vol. 64, no. 3, pp. 387–391, 2013.
View at: Google Scholar

Copyright

Copyright © 2021 Barbara Sampaio Dias Martins Mansano et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

PDF Download Citation

Download other formats

Order printed copies

Views

1858

Downloads

884

Citations