Skip to main content
Top
Published in: Lasers in Medical Science 3/2020

01-04-2020 | Laser | Original Article

Photobiomodulation therapy compensate the impairments of diabetic bone marrow mesenchymal stem cells

Authors: Fatemeh Zare, Mohammad Bayat, Abbas Aliaghaei, Abbas Piryaei

Published in: Lasers in Medical Science | Issue 3/2020

Login to get access

Abstract

Pathophysiologic conditions associated with diabetes mellitus affect mesenchymal stem cells (MSCs), and this phenomenon may lead to some diabetic secondary complications. The present study was conducted to evaluate the impact of photobiomodulation (PBM) on rat diabetic MSC (DMSC) behavior in vitro. For the purpose of PBM, we used helium-neon laser with a wavelength of 632.8 nm at three different energy densities (0.5, 1, 2 J/cm2) and radiation periodicity of once, twice, and thrice. The survival, proliferation, and apoptosis in the normal MSCs (NMSCs), DMSCs, and diabetic MSCs, which were laser irradiated (DMSCs+L), were assessed using MTT assay, Ki67 immunofluorescence staining, and TUNEL assay, respectively. Our results demonstrated that DMSCs have significantly lower survival (P < 0.05) and proliferation rates (P < 0.001), and dramatically higher population doubling time (PDT, P < 0.001) and apoptosis rates (P < 0.001) as compared to NMSCs. Moreover, PBM with energy density of 1 J/cm2 and the periodicity of 1 or 2 times could improve diabetic MSC capabilities in the term of survival, proliferation, and apoptosis. Considering these findings, it is suggested that PBM could improve the ability of diabetic MSCs in vitro prior to transplantation or may rise their capabilities in their native niche in vivo.
Literature
1.
go back to reference Guariguata L et al (2014) Global estimates of diabetes prevalence for 2013 and projections for 2035. Diabetes Res Clin Pract 103(2):137–149PubMedCrossRef Guariguata L et al (2014) Global estimates of diabetes prevalence for 2013 and projections for 2035. Diabetes Res Clin Pract 103(2):137–149PubMedCrossRef
2.
go back to reference Ogurtsova K et al (2017) IDF Diabetes Atlas: global estimates for the prevalence of diabetes for 2015 and 2040. Diabetes Res Clin Pract 128:40–50PubMedCrossRef Ogurtsova K et al (2017) IDF Diabetes Atlas: global estimates for the prevalence of diabetes for 2015 and 2040. Diabetes Res Clin Pract 128:40–50PubMedCrossRef
3.
go back to reference Mathis D, Vence L, Benoist C (2001) Beta-cell death during progression to diabetes. Nature 414(6865):792–798PubMedCrossRef Mathis D, Vence L, Benoist C (2001) Beta-cell death during progression to diabetes. Nature 414(6865):792–798PubMedCrossRef
5.
go back to reference Pittenger MF et al (1999) Multilineage potential of adult human mesenchymal stem cells. science 284(5411):143–147PubMedCrossRef Pittenger MF et al (1999) Multilineage potential of adult human mesenchymal stem cells. science 284(5411):143–147PubMedCrossRef
8.
go back to reference Chen W et al (2018) Angiogenic and osteogenic regeneration in rats via calcium phosphate scaffold and endothelial cell co-culture with human bone marrow mesenchymal stem cells (MSCs), human umbilical cord MSCs, human induced pluripotent stem cell-derived MSCs and human embryonic stem cell-derived MSCs. J Tissue Eng Regen Med 12(1):191–203PubMedCrossRef Chen W et al (2018) Angiogenic and osteogenic regeneration in rats via calcium phosphate scaffold and endothelial cell co-culture with human bone marrow mesenchymal stem cells (MSCs), human umbilical cord MSCs, human induced pluripotent stem cell-derived MSCs and human embryonic stem cell-derived MSCs. J Tissue Eng Regen Med 12(1):191–203PubMedCrossRef
9.
go back to reference Sackstein R et al (2008) Ex vivo glycan engineering of CD44 programs human multipotent mesenchymal stromal cell trafficking to bone. Nat Med 14(2):181PubMedCrossRef Sackstein R et al (2008) Ex vivo glycan engineering of CD44 programs human multipotent mesenchymal stromal cell trafficking to bone. Nat Med 14(2):181PubMedCrossRef
10.
go back to reference Laird DJ, von Andrian UH, Wagers AJ (2008) Stem cell trafficking in tissue development, growth, and disease. Cell 132(4):612–630PubMedCrossRef Laird DJ, von Andrian UH, Wagers AJ (2008) Stem cell trafficking in tissue development, growth, and disease. Cell 132(4):612–630PubMedCrossRef
11.
12.
go back to reference Bellin MD et al (2012) Potent induction immunotherapy promotes long-term insulin independence after islet transplantation in type 1 diabetes. Am J Transplant 12(6):1576–1583PubMedPubMedCentralCrossRef Bellin MD et al (2012) Potent induction immunotherapy promotes long-term insulin independence after islet transplantation in type 1 diabetes. Am J Transplant 12(6):1576–1583PubMedPubMedCentralCrossRef
13.
go back to reference Thakkar UG et al (2015) Insulin-secreting adipose-derived mesenchymal stromal cells with bone marrow–derived hematopoietic stem cells from autologous and allogenic sources for type 1 diabetes mellitus. Cytotherapy 17(7):940–947PubMedCrossRef Thakkar UG et al (2015) Insulin-secreting adipose-derived mesenchymal stromal cells with bone marrow–derived hematopoietic stem cells from autologous and allogenic sources for type 1 diabetes mellitus. Cytotherapy 17(7):940–947PubMedCrossRef
14.
go back to reference Wang Z-X et al (2015) Clinical efficacy of autologous stem cell transplantation for the treatment of patients with type 2 diabetes mellitus: a meta-analysis. Cytotherapy 17(7):956–968PubMedCrossRef Wang Z-X et al (2015) Clinical efficacy of autologous stem cell transplantation for the treatment of patients with type 2 diabetes mellitus: a meta-analysis. Cytotherapy 17(7):956–968PubMedCrossRef
16.
go back to reference Hendudari F et al (2016) Combined effects of low-level laser therapy and human bone marrow mesenchymal stem cell conditioned medium on viability of human dermal fibroblasts cultured in a high-glucose medium. Lasers Med Sci 31(4):749–757PubMedCrossRef Hendudari F et al (2016) Combined effects of low-level laser therapy and human bone marrow mesenchymal stem cell conditioned medium on viability of human dermal fibroblasts cultured in a high-glucose medium. Lasers Med Sci 31(4):749–757PubMedCrossRef
18.
go back to reference Gavish L et al (2008) Irradiation with 780 nm diode laser attenuates inflammatory cytokines but upregulates nitric oxide in lipopolysaccharide-stimulated macrophages: implications for the prevention of aneurysm progression. Lasers Surg Med 40(5):371PubMedCrossRef Gavish L et al (2008) Irradiation with 780 nm diode laser attenuates inflammatory cytokines but upregulates nitric oxide in lipopolysaccharide-stimulated macrophages: implications for the prevention of aneurysm progression. Lasers Surg Med 40(5):371PubMedCrossRef
19.
go back to reference Giannelli M et al (2013) Photoactivation of bone marrow mesenchymal stromal cells with diode laser: effects and mechanisms of action. J Cell Physiol 228(1):172–181PubMedCrossRef Giannelli M et al (2013) Photoactivation of bone marrow mesenchymal stromal cells with diode laser: effects and mechanisms of action. J Cell Physiol 228(1):172–181PubMedCrossRef
20.
go back to reference Rizzi CF et al (2006) Effects of low-level laser therapy (LLLT) on the nuclear factor (NF)-κB signaling pathway in traumatized muscle. Lasers Surg Med 38(7):704–713PubMedCrossRef Rizzi CF et al (2006) Effects of low-level laser therapy (LLLT) on the nuclear factor (NF)-κB signaling pathway in traumatized muscle. Lasers Surg Med 38(7):704–713PubMedCrossRef
21.
go back to reference Gasparyan L, Brill G, Makela A (2004) Influence of low level laser radiation on migration of stem cells. Laser Florence 2004:1–7 Gasparyan L, Brill G, Makela A (2004) Influence of low level laser radiation on migration of stem cells. Laser Florence 2004:1–7
22.
go back to reference Ayuk SM, Abrahamse H, Houreld NN (2018) Photobiomodulation alters matrix protein activity in stressed fibroblast cells in vitro. J Biophotonics 11(3):e201700127CrossRef Ayuk SM, Abrahamse H, Houreld NN (2018) Photobiomodulation alters matrix protein activity in stressed fibroblast cells in vitro. J Biophotonics 11(3):e201700127CrossRef
23.
go back to reference Ginani F, Soares DM, Barboza CAG (2015) Effect of low-level laser therapy on mesenchymal stem cell proliferation: a systematic review. Lasers Med Sci 30(8):2189–2194PubMedCrossRef Ginani F, Soares DM, Barboza CAG (2015) Effect of low-level laser therapy on mesenchymal stem cell proliferation: a systematic review. Lasers Med Sci 30(8):2189–2194PubMedCrossRef
24.
go back to reference Tsuka Y et al (2019) Effects of Nd: YAG low-level laser irradiation on cultured human osteoblasts migration and ATP production: in vitro study. Lasers Med Sci 34(1):55–60PubMedCrossRef Tsuka Y et al (2019) Effects of Nd: YAG low-level laser irradiation on cultured human osteoblasts migration and ATP production: in vitro study. Lasers Med Sci 34(1):55–60PubMedCrossRef
25.
go back to reference Eichler M et al (2007) Red light-induced redox reactions in cells observed with TEMPO. Photomed Laser Surg 25(3):170–174PubMedCrossRef Eichler M et al (2007) Red light-induced redox reactions in cells observed with TEMPO. Photomed Laser Surg 25(3):170–174PubMedCrossRef
26.
go back to reference Yin K et al (2017) Low-level laser effect on proliferation, migration, and antiapoptosis of mesenchymal stem cells. Stem Cells Dev 26(10):762–775PubMedCrossRef Yin K et al (2017) Low-level laser effect on proliferation, migration, and antiapoptosis of mesenchymal stem cells. Stem Cells Dev 26(10):762–775PubMedCrossRef
27.
go back to reference Li X et al (2014) Comprehensive characterization of four different populations of human mesenchymal stem cells as regards their immune properties, proliferation and differentiation. Int J Mol Med 34(3):695–704PubMedPubMedCentralCrossRef Li X et al (2014) Comprehensive characterization of four different populations of human mesenchymal stem cells as regards their immune properties, proliferation and differentiation. Int J Mol Med 34(3):695–704PubMedPubMedCentralCrossRef
28.
go back to reference Esmaeelinejad M et al (2014) The effects of low-level laser irradiation on cellular viability and proliferation of human skin fibroblasts cultured in high glucose mediums. Lasers Med Sci 29(1):121–129PubMedCrossRef Esmaeelinejad M et al (2014) The effects of low-level laser irradiation on cellular viability and proliferation of human skin fibroblasts cultured in high glucose mediums. Lasers Med Sci 29(1):121–129PubMedCrossRef
29.
go back to reference Piryaei A et al (2015) Ultrastructural maturation of human bone marrow mesenchymal stem cells-derived cardiomyocytes under alternative induction of 5-azacytidine. Cell Biol Int 39(5):519–530PubMedCrossRef Piryaei A et al (2015) Ultrastructural maturation of human bone marrow mesenchymal stem cells-derived cardiomyocytes under alternative induction of 5-azacytidine. Cell Biol Int 39(5):519–530PubMedCrossRef
30.
go back to reference Bullwinkel J et al (2006) Ki-67 protein is associated with ribosomal RNA transcription in quiescent and proliferating cells. J Cell Physiol 206(3):624–635PubMedCrossRef Bullwinkel J et al (2006) Ki-67 protein is associated with ribosomal RNA transcription in quiescent and proliferating cells. J Cell Physiol 206(3):624–635PubMedCrossRef
31.
go back to reference Bruno S, Darzynkiewicz Z (1992) Cell cycle dependent expression and stability of the nuclear protein detected by Ki-67 antibody in HL-60 cells. Cell Prolif 25(1):31–40PubMedCrossRef Bruno S, Darzynkiewicz Z (1992) Cell cycle dependent expression and stability of the nuclear protein detected by Ki-67 antibody in HL-60 cells. Cell Prolif 25(1):31–40PubMedCrossRef
32.
go back to reference Kyrylkova K et al (2012) Detection of apoptosis by TUNEL assay. In: Odontogenesis: Methods and Protocols, pp 41–47CrossRef Kyrylkova K et al (2012) Detection of apoptosis by TUNEL assay. In: Odontogenesis: Methods and Protocols, pp 41–47CrossRef
33.
go back to reference Jin P et al. (2010) Streptozotocin-induced diabetic rat–derived bone marrow mesenchymal stem cells have impaired abilities in proliferation, paracrine, antiapoptosis, and myogenic differentiation. Transplant Proc 42(7):2745–2752PubMedCrossRef Jin P et al. (2010) Streptozotocin-induced diabetic rat–derived bone marrow mesenchymal stem cells have impaired abilities in proliferation, paracrine, antiapoptosis, and myogenic differentiation. Transplant Proc 42(7):2745–2752PubMedCrossRef
34.
go back to reference Cianfarani F et al (2013) Diabetes impairs adipose tissue–derived stem cell function and efficiency in promoting wound healing. Wound Repair Regen 21(4):545–553PubMedCrossRef Cianfarani F et al (2013) Diabetes impairs adipose tissue–derived stem cell function and efficiency in promoting wound healing. Wound Repair Regen 21(4):545–553PubMedCrossRef
35.
go back to reference Zhao Y-F et al (2013) Osteogenic potential of bone marrow stromal cells derived from streptozotocin-induced diabetic rats. Int J Mol Med 31(3):614–620PubMedCrossRef Zhao Y-F et al (2013) Osteogenic potential of bone marrow stromal cells derived from streptozotocin-induced diabetic rats. Int J Mol Med 31(3):614–620PubMedCrossRef
36.
go back to reference Khan M et al (2010) Growth factor preconditioning increases the function of diabetes-impaired mesenchymal stem cells. Stem Cells Dev 20(1):67–75PubMedCrossRef Khan M et al (2010) Growth factor preconditioning increases the function of diabetes-impaired mesenchymal stem cells. Stem Cells Dev 20(1):67–75PubMedCrossRef
37.
go back to reference Yaochite JNU et al (2016) Multipotent mesenchymal stromal cells from patients with newly diagnosed type 1 diabetes mellitus exhibit preserved in vitro and in vivo immunomodulatory properties. Stem Cell Res Ther 7(1):14PubMedPubMedCentralCrossRef Yaochite JNU et al (2016) Multipotent mesenchymal stromal cells from patients with newly diagnosed type 1 diabetes mellitus exhibit preserved in vitro and in vivo immunomodulatory properties. Stem Cell Res Ther 7(1):14PubMedPubMedCentralCrossRef
39.
go back to reference Fallahnezhad S et al (2016) Low-level laser therapy with helium-neon laser improved viability of osteoporotic bone marrow-derived mesenchymal stem cells from ovariectomy-induced osteoporotic rats. J Biomed Opt 21(9):98002PubMedCrossRef Fallahnezhad S et al (2016) Low-level laser therapy with helium-neon laser improved viability of osteoporotic bone marrow-derived mesenchymal stem cells from ovariectomy-induced osteoporotic rats. J Biomed Opt 21(9):98002PubMedCrossRef
40.
go back to reference Cavalcanti MFXB et al (2015) Evaluation of the proliferative effects induced by low-level laser therapy in bone marrow stem cell culture. Photomed Laser Surg 33(12):610–616PubMedCrossRef Cavalcanti MFXB et al (2015) Evaluation of the proliferative effects induced by low-level laser therapy in bone marrow stem cell culture. Photomed Laser Surg 33(12):610–616PubMedCrossRef
41.
go back to reference Li W-T, Leu Y-C, Wu J-L (2010) Red-light light-emitting diode irradiation increases the proliferation and osteogenic differentiation of rat bone marrow mesenchymal stem cells. Photomed Laser Surg 28(S1):S-157–S-165CrossRef Li W-T, Leu Y-C, Wu J-L (2010) Red-light light-emitting diode irradiation increases the proliferation and osteogenic differentiation of rat bone marrow mesenchymal stem cells. Photomed Laser Surg 28(S1):S-157–S-165CrossRef
42.
go back to reference Huang Y-Y et al (2009) Biphasic dose response in low level light therapy. Dose Response 7(4):358-383 CrossRef Huang Y-Y et al (2009) Biphasic dose response in low level light therapy. Dose Response 7(4):358-383 CrossRef
43.
go back to reference Soares DM et al (2015) Effects of laser therapy on the proliferation of human periodontal ligament stem cells. Lasers Med Sci 30(3):1171–1174PubMedCrossRef Soares DM et al (2015) Effects of laser therapy on the proliferation of human periodontal ligament stem cells. Lasers Med Sci 30(3):1171–1174PubMedCrossRef
44.
go back to reference Soleimani 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(2):423–430PubMedCrossRef Soleimani 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(2):423–430PubMedCrossRef
45.
go back to reference Filip S, Mokrý J, Hruska I (2003) Adult stem cells and their importance in cell therapy. Folia Biol 49(1):9–14 Filip S, Mokrý J, Hruska I (2003) Adult stem cells and their importance in cell therapy. Folia Biol 49(1):9–14
Metadata
Title
Photobiomodulation therapy compensate the impairments of diabetic bone marrow mesenchymal stem cells
Authors
Fatemeh Zare
Mohammad Bayat
Abbas Aliaghaei
Abbas Piryaei
Publication date
01-04-2020
Publisher
Springer London
Keyword
Laser
Published in
Lasers in Medical Science / Issue 3/2020
Print ISSN: 0268-8921
Electronic ISSN: 1435-604X
DOI
https://doi.org/10.1007/s10103-019-02844-y

Other articles of this Issue 3/2020

Lasers in Medical Science 3/2020 Go to the issue