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Oladnabi M, Amir Mishan M, Rezaeikanavi M, Zargari M, Najjar Sadeghi R, Bagheri A. Correlation between ELF–PEMF exposure and Human RPE Cell Proliferation, Apoptosis and Gene Expression. JOVR [Internet]. 2021Apr.29 [cited 2024Apr.26];16(2):202–211. Available from: https://knepublishing.com/index.php/JOVR/article/view/9084
https://doi.org/10.18502/jovr.v16i2.9084
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authors
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Morteza Oladnabi
Morteza Oladnabi
Stem Cell Research Center, Golestan University of Medical Sciences, Gorgan, Iran
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Mohammad Amir Mishan
Mohammad Amir Mishan
Ocular Tissue Engineering Research Center, Research Institute for Ophthalmology and Vision Science, Shahid Beheshti University of Medical Sciences, Tehran, Iran
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Mozhgan Rezaeikanavi
Mozhgan Rezaeikanavi
Ocular Tissue Engineering Research Center, Research Institute for Ophthalmology and Vision Science, Shahid Beheshti University of Medical Sciences, Tehran, Iran
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Mehryar Zargari
Mehryar Zargari
Department of Clinical Biochemistry and Medical Genetics, Molecular and Cell Biology Research Center, Faculty of Medicine, Mazandaran University of Medical Sciences, Sari, Iran
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Rouhallah Najjar Sadeghi
Rouhallah Najjar Sadeghi
Department of Clinical Biochemistry and Medical Genetics, Molecular and Cell Biology Research Center, Faculty of Medicine, Mazandaran University of Medical Sciences, Sari, Iran
-
Abouzar Bagheri
Abouzar Bagheri
Department of Clinical Biochemistry and Medical Genetics, Molecular and Cell Biology Research Center, Faculty of Medicine, Mazandaran University of Medical Sciences, Sari, Iran
Published Date
- Apr 29, 2021
Correlation between ELF–PEMF exposure and Human RPE Cell Proliferation, Apoptosis and Gene Expression
Abstract
Purpose: Emerging evidence implies that electromagnetic fields (EMFs) can negatively affect angiogenesis. In this regard, the effects of extremely low frequency pulsed electromagnetic field (ELF–PEMF) exposure on the relative expression level of angiogenic factors involved in the pathogenesis of ocular disorders were evaluated in human retinal pigment epithelial (hRPE) cells in order to investigate a noninvasive therapeutic method for patients with several ocular diseases associated with neovascularization.
Methods: After separating hRPE cells from globes, hRPE cells were exposed to 15 mT of ELF–PEMF (120 Hz) at 5, 10, and 15 min for seven days. Cell proliferation and apoptosis of treated cells were evaluated via ELISA assay. Moreover, relative expression changes of HIF-1α, CTGF, VEGFA, MMP-2, cathepsin D, and E2F3 were performed using real-time RT-PCR.
Results: ELF–PEMF exposure had no significant effects on the apoptosis and proliferation rate of hRPE cells. Expression level of HIF-1α, CTGF, VEGFA, MMP- 2, cathepsin D, and E2F3 was downregulated following 5 min of ELF–PEMF exposure.
Conclusion: As ELF–PEMF showed inhibitory effects on the expression of angiogenic genes in hRPE cells with no cytotoxic or proliferative side effects, it can be introduced as a useful procedure for managing angiogenesis induced by retinal pathogenesis, although more studies with adequate follow-up in animal models are needed.
Keywords:
Angiogenic Factors, ELF–PEMFs, hRPE Cells
References
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2. Zhang Y, Cai S, Jia Y, Qi C, Sun J, Zhang H, et al. Decoding noncoding RNAs: role of microRNAs and long noncoding RNAs in ocular neovascularization. Theranostics 2017;7:3155.
3. Wong EN, Chew AL, Morgan WH, Patel PJ, Chen FK. The use of microperimetry to detect functional progression in non-neovascular age-related macular degeneration: a systematic review. Asia Pac J Ophthalmol 2017;6:70–79.
4. Ehlken C, Guichard M-M, Schlunck G, Bühler AD, Martin G, Agostini HT. Expression of angiogenic and inflammatory factors in choroidal neovascularisation-derived retinal pigment epithelium. Ophthalmic Res 2019;61:174–182.
5. Bagheri A, Soheili ZS, Ahmadieh H, Samiei S, Sheibani N, Astaneh SD, et al. Simultaneous application of bevacizumab and anti-CTGF antibody effectively suppresses proangiogenic and profibrotic factors in human RPE cells. Mol Vis 2015;21:378–390.
6. Heidari R, Soheili ZS, Samiei S, Ahmadieh H, Davari M, Nazemroaya F, et al. Alginate as a cell culture substrate for growth and differentiation of human retinal pigment epithelial cells. Appl Biochem Biotechnol 2015;175:2399– 2412.
7. Sanie-Jahromi F, Ahmadieh H, Soheili ZS, Davari M, Ghaderi S, Kanavi MR, et al. Enhanced generation of retinal progenitor cells from human retinal pigment epithelial cells induced by amniotic fluid. BMC Res Notes 2012;5:182.
8. Heirani-Tabasi A, Toosi S, Mirahmadi M, Mishan MA, Bidkhori HR, Bahrami AR. Chemokine receptors expression in MSCs: comparative analysis in different sources and passages. Tissue Eng Regen Med 2017;14:605–615.
9. Mirahmadi M, Ahmadiankia N, Naderi-Meshkin H, Heirani- Tabasi A, Bidkhori HR, Afsharian P, et al. Hypoxia and laser enhance expression of SDF-1 in muscles cells. Cell Mol Biol 2016;62:31–37.
10. Heirani-Tabasi A, Mirahmadi M, Mishan MA, Naderi- Meshkin H, Toosi S, Matin MM, et al. Comparison of the effects of hypoxia-mimicking agents on migration-related signaling pathways in mesenchymal stem cells. Cell Tissue Bank 2020;21:643–653.
11. André H, Tunik S, Aronsson M, Kvanta A. Hypoxiainducible factor-1α is associated with sprouting angiogenesis in the murine laser-induced choroidal neovascularization model. Invest Ophthalmol Vis Sci 2015;56:6591–6604.
12. Ved N, Hulse RP, Bestall SM, Donaldson LF, Bainbridge JW, Bates D. Vascular endothelial growth factor-A165b ameliorates outer-retinal barrier and vascular dysfunction in the diabetic retina. Clin Sci 2017;131:1225–1243.
13. Sun D, Nakao S, Xie F, Zandi S, Bagheri A, Kanavi MR, et al. Molecular imaging reveals elevated VEGFR-2 expression in retinal capillaries in diabetes: a novel biomarker for early diagnosis. FASEB J 2014;28:3942–3951.
14. Wheler JJ, Janku F, Naing A, Li Y, Stephen B, Zinner R, et al. TP53 Alterations correlate with response to VEGF/VEGFR inhibitors: implications for targeted therapeutics. Mol Cancer Ther 2016;15:2475–2485.
15. Klaassen I, van Geest RJ, Kuiper EJ, van Noorden CJ, Schlingemann RO. The role of CTGF in diabetic retinopathy. Exp Eye Res 2015;133:37–48.
16. Ishizaki E, Takai S, Ueki M, Maeno T, Maruichi M, Sugiyama T, et al. Correlation between angiotensin-converting enzyme, vascular endothelial growth factor, and matrix metalloproteinase-9 in the vitreous of eyes with diabetic retinopathy. Am J Ophthalmol 2006;141:129–134.
17. Vizovišek M, Fonović M, Turk B. Cysteine cathepsins in extracellular matrix remodeling: Extracellular matrix degradation and beyond. Matrix Biol 2018;75–76:141–159. 19. Shastry BS. Genetic susceptibility to advanced retinopathy of prematurity (ROP). J Biomed Sci 2010;17:69.
19. Chiavenna S, Jaworski J, Vendrell A. State of the art in anticancer mAbs. J Biomed Sci 2017;24:15. 20. Ye W. The complexity of translating anti-angiogenesis therapy from basic science to the clinic. Dev Cell 2016;37:114–125.
21. Iwase T, Fu J, Yoshida T, Muramatsu D, Miki A, Hashida N, et al. Sustained delivery of a HIF-1 antagonist for ocular neovascularization. J Control Release 2013;172:625–633.
22. Barnett JM, McCollum GW, Fowler JA, Duan JJ-W, Kay JD, Liu R-Q, et al. Pharmacologic and genetic manipulation of MMP-2 and-9 affects retinal neovascularization in rodent models of OIR. Invest Ophthalmol Vis Sci 2007;48:907– 915.
23. Markov MS. Magnetic field therapy: a review. Electromagn Biol Med 2007;26:1–23.
24. Ehnert S, Fentz A-K, Schreiner A, Birk J, Wilbrand B, Ziegler P, et al. Extremely low frequency pulsed electromagnetic fields cause antioxidative defense mechanisms in human osteoblasts via induction of O2− and H2O2. Sci Rep 2017;7:14544.
25. Kanavi MR, Tabeie F, Sahebjam F, Poursani N, Jahanbakhsh N, Paymanpour P, et al. Short-term effects of extremely low-frequency pulsed electromagnetic field and pulsed low-level laser therapy on rabbit model of corneal alkali burn. Exp Eye Res 2016;145:216–223.
26. Delle Monache S, Angelucci A, Sanità P, Iorio R, Bennato F, Mancini F, et al. Inhibition of angiogenesis mediated by extremely low-frequency magnetic fields (ELF-MFs). PLoS ONE 2013;8:e79309.
27. Akbarnejad Z, Eskandary H, Vergallo C, Nematollahi- Mahani SN, Dini L, Darvishzadeh-Mahani F, et al. Effects of extremely low-frequency pulsed electromagnetic fields (ELF–PEMFs) on glioblastoma cells (U87). Electromagn Biol Med 2017;36:238–247.
28. Nasrabadi N, Soheili ZS, Bagheri A, Ahmadieh H, Amizadeh Y, Sahebjam F, et al. The effects of electromagnetic fields on cultured human retinal pigment epithelial cells. Bioelectromagnetics 2018;39:585–594.
29. Campochiaro PA, Aiello LP, Rosenfeld PJ. Anti–vascular endothelial growth factor agents in the treatment of retinal disease: from bench to bedside. Ophthalmology 2016;123:S78–S88. 30. Campochiaro PA. Ocular neovascularization. J Mol Med 2013;91:311–321.
31. Miller JW, Le Couter J, Strauss EC, Ferrara N. Vascular endothelial growth factor a in intraocular vascular disease. Ophthalmology 2013;120:106–114.
32. Niu G, Chen X. Vascular endothelial growth factor as an anti-angiogenic target for cancer therapy. Curr Drug Targets 2010;11:1000–1017.
33. Ungvari Z, Valcarcel-Ares MN, Tarantini S, Yabluchanskiy A, Fülöp GA, Kiss T, et al. Connective tissue growth factor (CTGF) in age-related vascular pathologies. Geroscience 2017;39:491–498.
34. Akbari Kordkheyli V, Khonakdar Tarsi A, Mishan MA, Tafazoli A, Bardania H, Zarpou S, et al. Effects of quercetin on microRNAs: a mechanistic review. J Cell Biochem 2019;120:1–15.
35. Yang H, Huang Y, Chen X, Liu J, Lu Y, Bu L, et al. The role of CTGF in the diabetic rat retina and its relationship with VEGF and TGF-β2, elucidated by treatment with CTGFsiRNA. Acta Ophthalmol 2010;88:652–659.
36. Wu W, Zaal EA, Berkers CR, Lemeer S, Heck AJ. CTGF/VEGFA-activated fibroblasts promote tumor migration through micro-environmental modulation. Mol Cell Proteomics 2018;17:1502–1514.
37. Mongiat M, Andreuzzi E, Tarticchio G, Paulitti A. Extracellular matrix, a hard player in angiogenesis. Int J Mol Sci 2016;17:1822.
38. Sivakumar P, Kitson C, Jarai G. Modeling and measuring extracellular matrix alterations in fibrosis: challenges and perspectives for antifibrotic drug discovery. Connect Tissue Res 2019;60:62–70.
39. Vadalà M, Morales-Medina JC, Vallelunga A, Palmieri B, Laurino C, Iannitti T. Mechanisms and therapeutic effectiveness of pulsed electromagnetic field therapy in oncology. Cancer Med 2016;5:3128–3139.
40. Lucia U, Ponzetto A. Some thermodynamic considerations on low frequency electromagnetic waves effects on cancer invasion and metastasis. Physica A 2017;467:289– 295.
41. Cameron IL, Markov MS, Hardman WE. Optimization of a therapeutic electromagnetic field (EMF) to retard breast cancer tumor growth and vascularity. Cancer Cell Int 2014;14:125.
42. Yang X-S, He G-L, Hao Y-T, Xiao Y, Chen C-H, Zhang G-B, et al. Exposure to 2.45 GHz electromagnetic fields elicits an HSP-related stress response in rat hippocampus. Brain Res Bull 2012;88:371–378.
43. Robertson JA, Thomas AW, Bureau Y, Prato FS. The influence of extremely low frequency magnetic fields on cytoprotection and repair. Bioelectromagnetics 2007;28:16–30.
44. Delle Monache S, Alessandro R, Iorio R, Gualtieri G, Colonna R. Extremely low frequency electromagnetic fields (ELF-EMFs) induce in vitro angiogenesis process in human endothelial cells. Bioelectromagnetics 2008;29:640–648.
45. Bruns AF, Yuldasheva N, Latham AM, Bao L, Pellet- Many C, Frankel P, et al. A heat-shock protein axis regulates VEGFR2 proteolysis, blood vessel development and repair. PLoS ONE 2012;7:e48539.
46. Mousavi M, Baharara J, Shahrokhabadi K. The synergic effects of Crocus sativus L. and low frequency electromagnetic field on VEGFR2 gene expression in human breast cancer cells. Avicenna J Med Biotechnol 2014;6:123.
47. Li F, Lei T, Xie K, Wu X, Tang C, Jiang M, et al. Effects of extremely low frequency pulsed magnetic fields on diabetic nephropathy in streptozotocin-treated rats. Biomed Eng Online 2016;15:8.
48. Oladnabi M, Bagheri A, Rezaei Kanavi M, Azadmehr A, Kianmehr A. Extremely low frequency-pulsed electromagnetic fields affect proangiogenic-related gene expression in retinal pigment epithelial cells. Iran J Basic Med Sci 2019;22:128–133.
49. D’Angelo C, Costantini E, Kamal M, Reale M. Experimental model for ELF-EMF exposure: concern for human health. Saudi J Biol Sci 2015;22:75–84.
2. Zhang Y, Cai S, Jia Y, Qi C, Sun J, Zhang H, et al. Decoding noncoding RNAs: role of microRNAs and long noncoding RNAs in ocular neovascularization. Theranostics 2017;7:3155.
3. Wong EN, Chew AL, Morgan WH, Patel PJ, Chen FK. The use of microperimetry to detect functional progression in non-neovascular age-related macular degeneration: a systematic review. Asia Pac J Ophthalmol 2017;6:70–79.
4. Ehlken C, Guichard M-M, Schlunck G, Bühler AD, Martin G, Agostini HT. Expression of angiogenic and inflammatory factors in choroidal neovascularisation-derived retinal pigment epithelium. Ophthalmic Res 2019;61:174–182.
5. Bagheri A, Soheili ZS, Ahmadieh H, Samiei S, Sheibani N, Astaneh SD, et al. Simultaneous application of bevacizumab and anti-CTGF antibody effectively suppresses proangiogenic and profibrotic factors in human RPE cells. Mol Vis 2015;21:378–390.
6. Heidari R, Soheili ZS, Samiei S, Ahmadieh H, Davari M, Nazemroaya F, et al. Alginate as a cell culture substrate for growth and differentiation of human retinal pigment epithelial cells. Appl Biochem Biotechnol 2015;175:2399– 2412.
7. Sanie-Jahromi F, Ahmadieh H, Soheili ZS, Davari M, Ghaderi S, Kanavi MR, et al. Enhanced generation of retinal progenitor cells from human retinal pigment epithelial cells induced by amniotic fluid. BMC Res Notes 2012;5:182.
8. Heirani-Tabasi A, Toosi S, Mirahmadi M, Mishan MA, Bidkhori HR, Bahrami AR. Chemokine receptors expression in MSCs: comparative analysis in different sources and passages. Tissue Eng Regen Med 2017;14:605–615.
9. Mirahmadi M, Ahmadiankia N, Naderi-Meshkin H, Heirani- Tabasi A, Bidkhori HR, Afsharian P, et al. Hypoxia and laser enhance expression of SDF-1 in muscles cells. Cell Mol Biol 2016;62:31–37.
10. Heirani-Tabasi A, Mirahmadi M, Mishan MA, Naderi- Meshkin H, Toosi S, Matin MM, et al. Comparison of the effects of hypoxia-mimicking agents on migration-related signaling pathways in mesenchymal stem cells. Cell Tissue Bank 2020;21:643–653.
11. André H, Tunik S, Aronsson M, Kvanta A. Hypoxiainducible factor-1α is associated with sprouting angiogenesis in the murine laser-induced choroidal neovascularization model. Invest Ophthalmol Vis Sci 2015;56:6591–6604.
12. Ved N, Hulse RP, Bestall SM, Donaldson LF, Bainbridge JW, Bates D. Vascular endothelial growth factor-A165b ameliorates outer-retinal barrier and vascular dysfunction in the diabetic retina. Clin Sci 2017;131:1225–1243.
13. Sun D, Nakao S, Xie F, Zandi S, Bagheri A, Kanavi MR, et al. Molecular imaging reveals elevated VEGFR-2 expression in retinal capillaries in diabetes: a novel biomarker for early diagnosis. FASEB J 2014;28:3942–3951.
14. Wheler JJ, Janku F, Naing A, Li Y, Stephen B, Zinner R, et al. TP53 Alterations correlate with response to VEGF/VEGFR inhibitors: implications for targeted therapeutics. Mol Cancer Ther 2016;15:2475–2485.
15. Klaassen I, van Geest RJ, Kuiper EJ, van Noorden CJ, Schlingemann RO. The role of CTGF in diabetic retinopathy. Exp Eye Res 2015;133:37–48.
16. Ishizaki E, Takai S, Ueki M, Maeno T, Maruichi M, Sugiyama T, et al. Correlation between angiotensin-converting enzyme, vascular endothelial growth factor, and matrix metalloproteinase-9 in the vitreous of eyes with diabetic retinopathy. Am J Ophthalmol 2006;141:129–134.
17. Vizovišek M, Fonović M, Turk B. Cysteine cathepsins in extracellular matrix remodeling: Extracellular matrix degradation and beyond. Matrix Biol 2018;75–76:141–159. 19. Shastry BS. Genetic susceptibility to advanced retinopathy of prematurity (ROP). J Biomed Sci 2010;17:69.
19. Chiavenna S, Jaworski J, Vendrell A. State of the art in anticancer mAbs. J Biomed Sci 2017;24:15. 20. Ye W. The complexity of translating anti-angiogenesis therapy from basic science to the clinic. Dev Cell 2016;37:114–125.
21. Iwase T, Fu J, Yoshida T, Muramatsu D, Miki A, Hashida N, et al. Sustained delivery of a HIF-1 antagonist for ocular neovascularization. J Control Release 2013;172:625–633.
22. Barnett JM, McCollum GW, Fowler JA, Duan JJ-W, Kay JD, Liu R-Q, et al. Pharmacologic and genetic manipulation of MMP-2 and-9 affects retinal neovascularization in rodent models of OIR. Invest Ophthalmol Vis Sci 2007;48:907– 915.
23. Markov MS. Magnetic field therapy: a review. Electromagn Biol Med 2007;26:1–23.
24. Ehnert S, Fentz A-K, Schreiner A, Birk J, Wilbrand B, Ziegler P, et al. Extremely low frequency pulsed electromagnetic fields cause antioxidative defense mechanisms in human osteoblasts via induction of O2− and H2O2. Sci Rep 2017;7:14544.
25. Kanavi MR, Tabeie F, Sahebjam F, Poursani N, Jahanbakhsh N, Paymanpour P, et al. Short-term effects of extremely low-frequency pulsed electromagnetic field and pulsed low-level laser therapy on rabbit model of corneal alkali burn. Exp Eye Res 2016;145:216–223.
26. Delle Monache S, Angelucci A, Sanità P, Iorio R, Bennato F, Mancini F, et al. Inhibition of angiogenesis mediated by extremely low-frequency magnetic fields (ELF-MFs). PLoS ONE 2013;8:e79309.
27. Akbarnejad Z, Eskandary H, Vergallo C, Nematollahi- Mahani SN, Dini L, Darvishzadeh-Mahani F, et al. Effects of extremely low-frequency pulsed electromagnetic fields (ELF–PEMFs) on glioblastoma cells (U87). Electromagn Biol Med 2017;36:238–247.
28. Nasrabadi N, Soheili ZS, Bagheri A, Ahmadieh H, Amizadeh Y, Sahebjam F, et al. The effects of electromagnetic fields on cultured human retinal pigment epithelial cells. Bioelectromagnetics 2018;39:585–594.
29. Campochiaro PA, Aiello LP, Rosenfeld PJ. Anti–vascular endothelial growth factor agents in the treatment of retinal disease: from bench to bedside. Ophthalmology 2016;123:S78–S88. 30. Campochiaro PA. Ocular neovascularization. J Mol Med 2013;91:311–321.
31. Miller JW, Le Couter J, Strauss EC, Ferrara N. Vascular endothelial growth factor a in intraocular vascular disease. Ophthalmology 2013;120:106–114.
32. Niu G, Chen X. Vascular endothelial growth factor as an anti-angiogenic target for cancer therapy. Curr Drug Targets 2010;11:1000–1017.
33. Ungvari Z, Valcarcel-Ares MN, Tarantini S, Yabluchanskiy A, Fülöp GA, Kiss T, et al. Connective tissue growth factor (CTGF) in age-related vascular pathologies. Geroscience 2017;39:491–498.
34. Akbari Kordkheyli V, Khonakdar Tarsi A, Mishan MA, Tafazoli A, Bardania H, Zarpou S, et al. Effects of quercetin on microRNAs: a mechanistic review. J Cell Biochem 2019;120:1–15.
35. Yang H, Huang Y, Chen X, Liu J, Lu Y, Bu L, et al. The role of CTGF in the diabetic rat retina and its relationship with VEGF and TGF-β2, elucidated by treatment with CTGFsiRNA. Acta Ophthalmol 2010;88:652–659.
36. Wu W, Zaal EA, Berkers CR, Lemeer S, Heck AJ. CTGF/VEGFA-activated fibroblasts promote tumor migration through micro-environmental modulation. Mol Cell Proteomics 2018;17:1502–1514.
37. Mongiat M, Andreuzzi E, Tarticchio G, Paulitti A. Extracellular matrix, a hard player in angiogenesis. Int J Mol Sci 2016;17:1822.
38. Sivakumar P, Kitson C, Jarai G. Modeling and measuring extracellular matrix alterations in fibrosis: challenges and perspectives for antifibrotic drug discovery. Connect Tissue Res 2019;60:62–70.
39. Vadalà M, Morales-Medina JC, Vallelunga A, Palmieri B, Laurino C, Iannitti T. Mechanisms and therapeutic effectiveness of pulsed electromagnetic field therapy in oncology. Cancer Med 2016;5:3128–3139.
40. Lucia U, Ponzetto A. Some thermodynamic considerations on low frequency electromagnetic waves effects on cancer invasion and metastasis. Physica A 2017;467:289– 295.
41. Cameron IL, Markov MS, Hardman WE. Optimization of a therapeutic electromagnetic field (EMF) to retard breast cancer tumor growth and vascularity. Cancer Cell Int 2014;14:125.
42. Yang X-S, He G-L, Hao Y-T, Xiao Y, Chen C-H, Zhang G-B, et al. Exposure to 2.45 GHz electromagnetic fields elicits an HSP-related stress response in rat hippocampus. Brain Res Bull 2012;88:371–378.
43. Robertson JA, Thomas AW, Bureau Y, Prato FS. The influence of extremely low frequency magnetic fields on cytoprotection and repair. Bioelectromagnetics 2007;28:16–30.
44. Delle Monache S, Alessandro R, Iorio R, Gualtieri G, Colonna R. Extremely low frequency electromagnetic fields (ELF-EMFs) induce in vitro angiogenesis process in human endothelial cells. Bioelectromagnetics 2008;29:640–648.
45. Bruns AF, Yuldasheva N, Latham AM, Bao L, Pellet- Many C, Frankel P, et al. A heat-shock protein axis regulates VEGFR2 proteolysis, blood vessel development and repair. PLoS ONE 2012;7:e48539.
46. Mousavi M, Baharara J, Shahrokhabadi K. The synergic effects of Crocus sativus L. and low frequency electromagnetic field on VEGFR2 gene expression in human breast cancer cells. Avicenna J Med Biotechnol 2014;6:123.
47. Li F, Lei T, Xie K, Wu X, Tang C, Jiang M, et al. Effects of extremely low frequency pulsed magnetic fields on diabetic nephropathy in streptozotocin-treated rats. Biomed Eng Online 2016;15:8.
48. Oladnabi M, Bagheri A, Rezaei Kanavi M, Azadmehr A, Kianmehr A. Extremely low frequency-pulsed electromagnetic fields affect proangiogenic-related gene expression in retinal pigment epithelial cells. Iran J Basic Med Sci 2019;22:128–133.
49. D’Angelo C, Costantini E, Kamal M, Reale M. Experimental model for ELF-EMF exposure: concern for human health. Saudi J Biol Sci 2015;22:75–84.