Photobiomodulation Therapy Improves Inflammatory Responses by Modifying Stereological Parameters, microRNA-21 and FGF2 Expression Photobiomodulation improves inflammatory responses
Journal of Lasers in Medical Sciences,
Vol. 14 (2023),
29 January 2023
,
Page e16
Abstract
Introduction: Photobiomodulation treatment (PBMT) is a relatively invasive method for treating wounds. An appropriate type of PBMT can produce desired and directed cellular and molecular processes. The aim of this study was to investigate the impacts of PBMT on stereological factors, bacterial count, and the expression of microRNA-21 and FGF2 in an infected, ischemic, and delayed wound healing model in rats with type one diabetes mellitus.
Methods: A delayed, ischemic, and infected wound was produced on the back skin of all 24 DM1 rats. Then, they were put into 4 groups at random (n=6 per group): 1=Control group day4 (CG day4); 2=Control group day 8 (CG day8); 3=PBMT group day4 (PGday 4), in which the rats were exposed to PBMT and killed on day 4; 4=PBMT group day8 (PGday8), in which the rats received PBMT and were killed on day 8. The size of the wound, the number of microbial colonies, stereological parameters, and the expression of microRNA-21 and FGF2 were all assessed in this study throughout the inflammation (day 4) and proliferation (day 8) stages of wound healing.
Results: On days 4 and 8, we discovered that the PGday4 and PGday8 groups significantly improved stereological parameters in comparison with the same CG groups. In terms of ulcer area size and microbiological counts, the PGday4 and PGday8 groups performed much better than the same CG groups. Simultaneously, the biomechanical findings in the PGday4 and PGday8 groups were much more extensive than those in the same CG groups. On days 4 and 8, the expression of FGF2 and microRNA-21 was more in all PG groups than in the CG groups (P<0.01).
Conclusion: PBMT significantly speeds up the repair of ischemic and MARS-infected wounds in DM1 rats by lowering microbial counts and modifying stereological parameters, microRNA-21, and FGF2 expression.
Keywords:
- Type one diabetes mellitus; Ulcer healing; Photobiomodulation; Stereological parameters; Microbial examination
How to Cite
Amini, A., Ghasemi Moravej, F., Mostafavinia, A. ., Ahmadi, H. ., Chien, S. ., & Bayat, M. . (2023). Photobiomodulation Therapy Improves Inflammatory Responses by Modifying Stereological Parameters, microRNA-21 and FGF2 Expression: Photobiomodulation improves inflammatory responses. Journal of Lasers in Medical Sciences, 14, e16. Retrieved from https://journals.sbmu.ac.ir/jlms/article/view/40643
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25. Moradi A, Kheirollahkhani Y, Fatahi P, et al. An improvement in acute wound healing in mice by the combined application of photobiomodulation and curcumin-loaded iron particles. Lasers in medical science 2019;34(4):779-791
26. Dompe C, Moncrieff L, Matys J, et al. Photobiomodulation—underlying mechanism and clinical applications. Journal of clinical medicine 2020;9(6):1724
27. Da Silva D, Crous A, Abrahamse H. Photobiomodulation: an effective approach to enhance proliferation and differentiation of adipose-derived stem cells into osteoblasts. Stem Cells International 2021;2021(
28. Crous A, van Rensburg MJ, Abrahamse H. Single and consecutive application of near-infrared and green irradiation modulates adipose derived stem cell proliferation and affect differentiation factors. Biochimie 2022;196(225-233
29. Zare F, Moradi A, Fallahnezhad S, et al. 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 2019;201(111658, doi:10.1016/j.jphotobiol.2019.111658
30. Edwards R, Harding KG. Bacteria and wound healing. Current opinion in infectious diseases 2004;17(2):91-96
31. Boulton AJ, Armstrong DG, Kirsner RS, et al. Diagnosis and management of diabetic foot complications. 2018;
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33. Mot YY, Othman I, Sharifah SH. Synergistic antibacterial effect of co-administering adipose-derived mesenchymal stromal cells and Ophiophagus hannah l-amino acid oxidase in a mouse model of methicillin-resistant Staphylococcus aureus-infected wounds. Stem cell research & therapy 2017;8(1):5
34. Ranjbar R, Takhtfooladi MA. The effects of low level laser therapy on Staphylococcus aureus infected third-degree burns in diabetic rats. Acta cirurgica brasileira 2016;31(4):250-5, doi:10.1590/s0102-865020160040000005
35. Lipovsky A, Nitzan Y, Gedanken A, et al. Visible light‐induced killing of bacteria as a function of wavelength: Implication for wound healing. Lasers in surgery and medicine 2010;42(6):467-472
36. Fridoni M, Kouhkheil R, Abdollhifar MA, et al. Improvement in infected wound healing in type 1 diabetic rat by the synergistic effect of photobiomodulation therapy and conditioned medium. 2019;120(6):9906-9916, doi:10.1002/jcb.28273
37. Kim H, Kim DE, Han G, et al. Harnessing the Natural Healing Power of Colostrum: Bovine Milk‐Derived Extracellular Vesicles from Colostrum Facilitating the Transition from Inflammation to Tissue Regeneration for Accelerating Cutaneous Wound Healing. Advanced Healthcare Materials 2022;11(6):2102027
38. Madhyastha R, Madhyastha H, Nakajima Y, et al. MicroRNA signature in diabetic wound healing: promotive role of miR‐21 in fibroblast migration. International wound journal 2012;9(4):355-361
39. Ahmadi H, Amini A, Fadaei Fathabady F, et al. Transplantation of photobiomodulation-preconditioned diabetic stem cells accelerates ischemic wound healing in diabetic rats. Stem cell research & therapy 2020;11(1):494, doi:10.1186/s13287-020-01967-2
40. Geiger A, Walker A, Nissen E. Human fibrocyte-derived exosomes accelerate wound healing in genetically diabetic mice. Biochemical and biophysical research communications 2015;467(2):303-309
41. Roy S, Sen CK. miRNA in wound inflammation and angiogenesis. Microcirculation 2012;19(3):224-232
42. Trzyna A, Banaś-Ząbczyk A. Adipose-derived stem cells secretome and its potential application in “stem cell-free therapy”. Biomolecules 2021;11(6):878
43. Li Q, Zhao H, Chen W, et al. Human keratinocyte-derived microvesicle miRNA-21 promotes skin wound healing in diabetic rats through facilitating fibroblast function and angiogenesis. The international journal of biochemistry & cell biology 2019;114(105570
44. Raziyeva K, Kim Y, Zharkinbekov Z, et al. Immunology of acute and chronic wound healing. Biomolecules 2021;11(5):700
2. Catrina SB, Zheng X. Disturbed hypoxic responses as a pathogenic mechanism of diabetic foot ulcers. Diabetes/metabolism research and reviews 2016;32 Suppl 1(179-85, doi:10.1002/dmrr.2742
3. Brancato SK, Albina JE. Wound macrophages as key regulators of repair: origin, phenotype, and function. The American journal of pathology 2011;178(1):19-25
4. Duraisamy Y, Slevin M, Smith N, et al. Effect of glycation on basic fibroblast growth factor induced angiogenesis and activation of associated signal transduction pathways in vascular endothelial cells: possible relevance to wound healing in diabetes. Angiogenesis 2001;4(4):277-288
5. Grazul-Bilska A, Luthra G, Reynolds L, et al. Effects of basic fibroblast growth factor (FGF-2) on proliferation of human skin fibroblasts in type II diabetes mellitus. Experimental and clinical endocrinology & diabetes 2002;110(04):176-181
6. Wolf L, Gao CS, Gueta K, et al. Identification and characterization of FGF2-dependent mRNA: microRNA networks during lens fiber cell differentiation. G3: Genes, Genomes, Genetics 2013;3(12):2239-2255
7. Li D, Landén NX. MicroRNAs in skin wound healing. European journal of dermatology : EJD 2017;27(S1):12-14, doi:10.1684/ejd.2017.3040
8. Xie J, Wu W, Zheng L, et al. Roles of MicroRNA-21 in Skin Wound Healing: A Comprehensive Review. Frontiers in Pharmacology 2022;13(
9. Bhatt K, Lanting LL, Jia Y, et al. Anti-inflammatory role of microRNA-146a in the pathogenesis of diabetic nephropathy. Journal of the American Society of Nephrology 2016;27(8):2277-2288
10. Sekar D, Venugopal B, Sekar P, et al. Role of microRNA 21 in diabetes and associated/related diseases. Gene 2016;582(1):14-18
11. Liechty C, Hu J, Zhang L, et al. Role of microRNA-21 and its underlying mechanisms in inflammatory responses in diabetic wounds. International Journal of Molecular Sciences 2020;21(9):3328
12. Roy D, Modi A, Khokhar M, et al. Microrna 21 emerging role in diabetic complications: a critical update. Current diabetes reviews 2021;17(2):122-135
13. Cury V, Moretti AIS, Assis L, et al. Low level laser therapy increases angiogenesis in a model of ischemic skin flap in rats mediated by VEGF, HIF-1α and MMP-2. Journal of Photochemistry and Photobiology B: Biology 2013;125(164-170
14. Ahmadi H, Amini A, Fadaei Fathabady F, et al. Transplantation of photobiomodulation-preconditioned diabetic stem cells accelerates ischemic wound healing in diabetic rats. Stem cell research & therapy 2020;11(1):1-14
15. Park I-S, Mondal A, Chung P-S, et al. Prevention of skin flap necrosis by use of adipose-derived stromal cells with light-emitting diode phototherapy. Cytotherapy 2015;17(3):283-292
16. Karu T. Is it time to consider photobiomodulation as a drug equivalent? Mary Ann Liebert, Inc. 140 Huguenot Street, 3rd Floor New Rochelle, NY 10801 USA: 2013.
17. Saltmarche AE. Low level laser therapy for healing acute and chronic wounds–the extendicare experience. International Wound Journal 2008;5(2):351-360
18. Fallahnezhad S, Piryaei A, Tabeie F, et al. 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 2016;21(9):098002
19. Brem H, Tomic-Canic M. Cellular and molecular basis of wound healing in diabetes. The Journal of clinical investigation 2007;117(5):1219-1222
20. Moradi A, Zare F, Mostafavinia A, et al. Photobiomodulation plus adipose-derived stem cells improve healing of ischemic infected wounds in type 2 diabetic rats. Scientific Reports 2020;10(1):1-15
21. Mostafavinia A, Amini A, Ghorishi SK, et al. The effects of dosage and the routes of administrations of streptozotocin and alloxan on induction rate of type1 diabetes mellitus and mortality rate in rats. Laboratory animal research 2016;32(3):160-165, doi:10.5625/lar.2016.32.3.160
22. Pouriran R, Piryaei A, Mostafavinia A, et al. The Effect of Combined Pulsed Wave Low-Level Laser Therapy and Human Bone Marrow Mesenchymal Stem Cell-Conditioned Medium on Open Skin Wound Healing in Diabetic Rats. Photomedicine and laser surgery 2016;34(8):345-54, doi:10.1089/pho.2015.4020
23. Kouhkheil R, Fridoni M, Piryaei A. The effect of combined pulsed wave low-level laser therapy and mesenchymal stem cell-conditioned medium on the healing of an infected wound with methicillin-resistant Staphylococcal aureus in diabetic rats. 2018;119(7):5788-5797, doi:10.1002/jcb.26759
24. Kouhkheil R, Fridoni M, Abdollhifar M-A, et al. Impact of photobiomodulation and condition medium on mast cell counts, degranulation, and wound strength in infected skin wound healing of diabetic rats. Photobiomodulation, photomedicine, and laser surgery 2019;37(11):706-714
25. Moradi A, Kheirollahkhani Y, Fatahi P, et al. An improvement in acute wound healing in mice by the combined application of photobiomodulation and curcumin-loaded iron particles. Lasers in medical science 2019;34(4):779-791
26. Dompe C, Moncrieff L, Matys J, et al. Photobiomodulation—underlying mechanism and clinical applications. Journal of clinical medicine 2020;9(6):1724
27. Da Silva D, Crous A, Abrahamse H. Photobiomodulation: an effective approach to enhance proliferation and differentiation of adipose-derived stem cells into osteoblasts. Stem Cells International 2021;2021(
28. Crous A, van Rensburg MJ, Abrahamse H. Single and consecutive application of near-infrared and green irradiation modulates adipose derived stem cell proliferation and affect differentiation factors. Biochimie 2022;196(225-233
29. Zare F, Moradi A, Fallahnezhad S, et al. 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 2019;201(111658, doi:10.1016/j.jphotobiol.2019.111658
30. Edwards R, Harding KG. Bacteria and wound healing. Current opinion in infectious diseases 2004;17(2):91-96
31. Boulton AJ, Armstrong DG, Kirsner RS, et al. Diagnosis and management of diabetic foot complications. 2018;
32. Smith TL, Pearson ML, Wilcox KR, et al. Emergence of vancomycin resistance in Staphylococcus aureus. New England Journal of Medicine 1999;340(7):493-501
33. Mot YY, Othman I, Sharifah SH. Synergistic antibacterial effect of co-administering adipose-derived mesenchymal stromal cells and Ophiophagus hannah l-amino acid oxidase in a mouse model of methicillin-resistant Staphylococcus aureus-infected wounds. Stem cell research & therapy 2017;8(1):5
34. Ranjbar R, Takhtfooladi MA. The effects of low level laser therapy on Staphylococcus aureus infected third-degree burns in diabetic rats. Acta cirurgica brasileira 2016;31(4):250-5, doi:10.1590/s0102-865020160040000005
35. Lipovsky A, Nitzan Y, Gedanken A, et al. Visible light‐induced killing of bacteria as a function of wavelength: Implication for wound healing. Lasers in surgery and medicine 2010;42(6):467-472
36. Fridoni M, Kouhkheil R, Abdollhifar MA, et al. Improvement in infected wound healing in type 1 diabetic rat by the synergistic effect of photobiomodulation therapy and conditioned medium. 2019;120(6):9906-9916, doi:10.1002/jcb.28273
37. Kim H, Kim DE, Han G, et al. Harnessing the Natural Healing Power of Colostrum: Bovine Milk‐Derived Extracellular Vesicles from Colostrum Facilitating the Transition from Inflammation to Tissue Regeneration for Accelerating Cutaneous Wound Healing. Advanced Healthcare Materials 2022;11(6):2102027
38. Madhyastha R, Madhyastha H, Nakajima Y, et al. MicroRNA signature in diabetic wound healing: promotive role of miR‐21 in fibroblast migration. International wound journal 2012;9(4):355-361
39. Ahmadi H, Amini A, Fadaei Fathabady F, et al. Transplantation of photobiomodulation-preconditioned diabetic stem cells accelerates ischemic wound healing in diabetic rats. Stem cell research & therapy 2020;11(1):494, doi:10.1186/s13287-020-01967-2
40. Geiger A, Walker A, Nissen E. Human fibrocyte-derived exosomes accelerate wound healing in genetically diabetic mice. Biochemical and biophysical research communications 2015;467(2):303-309
41. Roy S, Sen CK. miRNA in wound inflammation and angiogenesis. Microcirculation 2012;19(3):224-232
42. Trzyna A, Banaś-Ząbczyk A. Adipose-derived stem cells secretome and its potential application in “stem cell-free therapy”. Biomolecules 2021;11(6):878
43. Li Q, Zhao H, Chen W, et al. Human keratinocyte-derived microvesicle miRNA-21 promotes skin wound healing in diabetic rats through facilitating fibroblast function and angiogenesis. The international journal of biochemistry & cell biology 2019;114(105570
44. Raziyeva K, Kim Y, Zharkinbekov Z, et al. Immunology of acute and chronic wound healing. Biomolecules 2021;11(5):700
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