Top

Published in:

01-02-2020 | Laser | Original Article

Photobiomodulation increases cell viability via AKT activation in an in vitro model of diabetes induced by glucose neurotoxicity

Authors: Victória Regina da Silva Oliveira, Rosangela Aparecida Santos-Eichler, Camila Squarzoni Dale

Published in: Lasers in Medical Science | Issue 1/2020

Abstract

Peripheral neuropathy (PN) is a serious complication of diabetes mellitus (DM) and is known to be resistant to conventional treatment. Photobiomodulation (PBM) is demonstrated to be effective in treating PN and in protecting nerve fiber damage. To better understand the mechanisms underlying the regenerative effects of PBM on diabetic neuropathy, we conducted a study in an in vitro model of diabetes induced by glucose neurotoxicity. Neuro 2A cells (1 × 10⁴ cells/ well; N2A) were cultured in Minimum Essential Medium (MEM) supplemented with high glucose concentrations (100 mM) for 48 h and after the incubation period were submitted to either one or three consecutive applications of PBM, once a day (low-level InGaAlP, continuous wave mode, 660 nm, 30 mW, 1.6 J/cm², 15 s, per well). Cell viability was measured by MTT method, neurotoxicity by LDH release, neurite outgrowth was evaluated through morphometric analysis, and AKT/ERK protein expression levels were assessed by western blotting. Results demonstrate that PBM increased N2A viability as well as induced neurogenesis observed by the increase in neurite outgrowth being this effect modulated by AKT activation. Data obtained herein reinforce the regenerative potential of PBM in the treatment of PN and strongly suggests that phototherapy should be considered adjuvant in the treatment of diabetes.

International Diabetes Federation-IDF (2017) Diabetes Atlas; 8th ed. Available from:http://www.idf.org/diabetesatlas

Toth CC, Jedrzejewski NM, Ellis CL, Frey WH (2010) Cannabinoid-mediated modulation of neuropathic pain and microglial accumulation in a model of murine type I diabetic peripheral neuropathic pain. Mol Pain 6:16CrossRef

Yerra VG, Kalvala AK, Sherkhane B, Areti A, Kumar A (2018) Adenosine monophosphate activated protein kinase modulation by berberine attenuates mitochondrial deficits and redox imbalance in experimental diabetic neuropathy. Neuropharmacology 131:256–270. https://doi.org/10.1016/j.neuropharm.2017.12.029 CrossRefPubMed

Barret AM, Lucero MA, Le T, Robinson RL, Dworkin RH, Chappell AS (2007) Epidemiology, public health burden, and treatment of diabetic peripheral neuropathic pain: a review. Pain Med 8:50–62. https://doi.org/10.1111/j.1526-4637.2006.00179.x CrossRef

Cao XH, Byun HS, Chen SR, Cai YQ, Pan HL (2010) Reduction in voltage-gated K+ channel activity in primary sensory neurons in painful diabetic neuropathy: role of brain derived neurotrophic factor. J Neurochem 114(5):1460–1475. https://doi.org/10.1111/j.1471-4159.2010.06863.x CrossRefPubMedPubMedCentral

Rondón LJ, Privat AM, Daulhac L, Davin N, Mazur A, Fialip J, Eschalier A, Courteix C (2010) Magnesium attenuates chronic hypersensitivity and spinal cord NMDA receptor phosphorylation in a rat model of diabetic neuropathic pain. J Physiol, 588(Pt 21):4205–4215. https://doi.org/10.1113/jphysiol.2010.197004 CrossRef

Said G (2007) Diabetic neuropathy—a review. Nat Clin Pract Neurol 3(6):331–340CrossRef

Tomlinson DR, Gardiner NJ (2008) Glucose neurotoxicity. Nat Rev Neurosci 9:36–45CrossRef

Mello JB, Mello GPS (2001) Tipos de lasers e indicações. In: Mello JB, Mello GPS. Laser em Odontologia. 1ª ed. São Paulo: Ed. Santos, pp 41–51

10.

Ortiz MCS, Matiello-Rosa SM, Soares EG, Parizotto NA (2003) Influência do laser de baixa potência nos níveis de proteínas plasmáticas de coelho. RevistaBrasileira de Fisioterapia 3:87–194

11.

Gál P, Mokrý M, Vidinský B, Kiík R, Depta F, Harakalová M, Longauer F, Mozes S, Sabo J (2009) Effect of equal daily doses achieved by different power densities of low-level laser therapy at 635 nm on open skin wound healing in normal and corticosteroid-treated rats. Lasers Med Sci (4):539–547CrossRef

12.

Wu SN, Xing D (2014) Intracellular signaling cascades following light irradiation. Laser Photonics Rev 8:115–130CrossRef

13.

Shefer G, Partridge TA, Heslop L, Gross JG, Oron U, Halevy O (2002) Low-energy laser irradiation promotes the survival and cell cycle entry of skeletal muscle satellite cells. J Cell Sci 115:1461–1469PubMed

14.

Jia YL, Guo ZY (2004) Effect of low-power He-Ne laser irradiation on rabbit articular chondrocytes in vitro. Lasers Surg Med 34:323–328CrossRef

15.

Fukuzaki Y, Sugawara H, Yamanoha B, Kogure S (2013) 532 nm low-power laser irradiation recovers γ-secretase inhibitor-mediated cell growth suppression and promotes cell proliferation via Akt signaling. PLoS One 8(8):e70737. https://doi.org/10.1371/journal.pone.0070737 CrossRef

16.

Huang L, Jiang X, Gong L, Xing D (2015) Photoactivation of Akt1/GSK3b isoform-specific signaling axis promotes pancreatic b-cell regeneration. J Cell Biochem 116:1741–1754CrossRef

17.

Yang J, Chen L, Yang J, Ding J, Rong H, Dong W, Li X (2012) High mobility group induces migration of vascular smooth muscle cells via TLR4-dependent PI3K/Akt pathway activation. Mol Biol Rep 39(3):3361–3367CrossRef

18.

Zhou B, Tan P, Jia L, Zhao W, Wang J, Wang H (2018) PI3K/AKT signaling pathway involvement in fluoride-induced apoptosis in C2C12 cells. Chemosphere 199:297–302CrossRef

19.

Liu G, Deng C (2017) The PI3K/Akt Signalling pathway plays essential roles in mesenchymal stem cells. Br Biomed Bull 5:301

20.

Mirzaei M, Bayat M, Mosafa N, Mohsenifar Z, Piryaei A, Farokhi B, Rezaei F, Sadeghi Y, Rakhshan M (2007) Effect of low-level laser therapy on skin fibroblasts of streptozotocin-diabetic rats. Photomed Laser Surg 25(6):519–525CrossRef

21.

Khamseh ME, Kazemikho N, Aghili R, Forough B, Lajevardi M, Dabaghian FH, Goushegir A, Malek M (2011) Diabetic distal symmetric polyneuropathy: effect of low-intensity laser therapy. Lasers Med Sci 26(6):831–835CrossRef

22.

Da Silva AA, Leal- Junior ECP, Alves ACA, Rambo CS, Santos SA, Vieira RP, Carvalho PTC (2013) Wound-healing effects of low-level laser therapy in diabetic rats involve the modulation of MMP-2 and MMP-9 and the redistribution of collagen types I and III. J Cosmet Laser Ther 15:210–216CrossRef

23.

Da Silva Oliveira VR, Cury DP, Yamashita LB, Esteca MV, Watanabe I, Bergmann YF, Toniolo EF, Dale CS (2018) Photobiomodulation induces antinociception, recovers structural aspects and regulates mitochondrial homeostasis in peripheral nerve of diabetic mice. J Biophotonics 2018; e201800110

24.

Yerra VG, Areti A, Kumar A (2017) Adenosine monophosphate-activated protein kinase abates Hyperglycaemia-induced neuronal injury in experimental models of diabetic neuropathy: effects on mitochondrial biogenesis, autophagy and neuroinflammation. MolNeurobiol 54(3):2313–2314. https://doi.org/10.1007/s12035-016-0183-x CrossRef

25.

Ueta C, Campos JC, Prestes E, Albuquerque R, Lima VM, Disatnik MH, Sanchez AB, Chen CH, Gennari De Medeiros MH, Yang W, Mochly-Rosen D, Batista Ferreira JC (2018) Cardioprotection induced by a brief exposure to acetaldehyde: role of aldehyde dehydrogenase 2. Cardiovasc Res 114(7):1006–1015CrossRef

26.

Ren C, Mcgrath C, Jin L, Zhang C, Yang Y (2016) Effect of diode low-level lasers on fibroblasts derived from human periodontal tissue: a systematic review of in vitro studies. Lasers Med Sci 31:1–18CrossRef

27.

Lou Z, Zhang C, Gong T, Xue C, Scholp A, Jiang JJ (2019) Wound-healing effects of 635-nm low-level laser therapy on primary human vocal fold epithelial cells: an in vitro study. Lasers Med Sci 34(3):547–554. https://doi.org/10.1007/s10103-018-2628-0 CrossRef

28.

Da Silva JP, Da Silva MA, Almeida AP, Lombardi Junior I, Matos AP (2010) Laser therapy in the tissue repair process: a literature review. Photomed Laser Surg 28:17–21CrossRef

29.

Eells JT, Henry MM, Summerfelt P, Wong-Riley MT, Buchmann EV, Kane M (2003) Therapeutic photobiomodulation for methanol-induced retinal toxicity. Proc Natl AcadSci USA 100(6):3439–3444CrossRef

30.

Asahi M, Yamamura H (1997) Physiological roles of cyclic nucleotide dependent protein kinases in advanced brain functions. Tanpakushitsu Kakusan Koso 42(3Suppl):403–410PubMed

31.

Yu HS, Chang KL, Yu CL, Chen JW, Chen GS (1996) Low-energy helium-neon laser irradiation stimulates interleukin-1 alpha and interleukin-8 release from cultured human keratinocytes. J Invest Dermatol 107:593–596CrossRef

32.

Conlan MJ, Rapley JW, Cobb CM (1996) Biostimulation of wound healing by low-energy laser irradiation. A review. J Clin Periodontol 23:492–496CrossRef

33.

Garcez AS, Ribeiro MS, Núñez SC (2012) Laser de Baixa Potência – Princípios básicos e aplicações clínicas na odontologia. Elsevier, Rio de Janeiro, p 259p

34.

Yerra VG, Kalvala AK, Kumar A (2017) Isoliquiritigenin reduces oxidative damage and alleviates mitochondrial impairment by SIRT1 activation in experimental diabetic neuropathy. J Nutr Biochem 47:41–52CrossRef

35.

Ayuk SM, Houreld NN, Abrahamse H (2018) Effect of 660 nm visible red light on cell proliferation and viability in diabetic models in vitro under stressed conditions. Lasers Med Sci 33:1085–1093. https://doi.org/10.1007/s10103-017-2432-2 CrossRefPubMed

36.

Janzadeh A, Nasirinezhad F, Masoumipoor M, Jameie SB, Hayat P (2016) Photobiomodulation therapy reduces apoptotic factors and increases glutathione levels in a neuropathic pain model. Lasers Med Sci 31(9):1863–1869CrossRef

37.

Peplow PV, Chung TY, Baxter GD (2012) Laser photostimulation (660 nm) of wound healing in diabetic mice is not brought about by ameliorating diabetes. Lasers Surg Med 44(1):26–29CrossRef

38.

Houreld NN, Ayuk SM, Abrahamse H (2018) Cell adhesion molecules are mediated by photobiomodulation at 660 nm in diabetic wounded fibroblast cells. Cells 7:30. https://doi.org/10.3390/cells7040030 CrossRefPubMedCentral

39.

Winner B, Kohl Z, Gage FH (2011) Neurodegenerative disease and adult neurogenesis. Eur J Neurosci 33:1139–1151CrossRef

40.

Ristow M (2004) Neurodegenerative disorders associated with diabetes mellitus. J Mol Med (Berl) 82(8):510–529CrossRef

41.

Gustafsson H, Söderdahl T, Jönsson G, Bratteng JO, Forsby A (2004) Insulin-like growth factor type 1 prevents hyperglycemia induced uncoupling protein 3 down-regulation and oxidative stress. J Neurosci Res 77(2):285–291CrossRef

42.

McAllister AK (2001) Neurotrophins and neuronal differentiation in the central nervous system. CMLS Cell Mol Life Sci 58:1054–1060CrossRef

43.

Mason EF, Rathmell JC (2011) Cell metabolism: an essential link between cell growth and apoptosis. Biochim Biophys Acta 1813:645–654CrossRef

44.

Boppart MD, Burkin DJ, Kaufman SJ (2011) Activation of Akt signaling promotes cell growth and survival in alpha7beta1 integrin-mediated alleviation of muscular dystrophy. Biochim Biophys Acta 1812:439–446CrossRef

45.

Hein AL, Ouellette MM, Ya Y (2014) Radiation-induced signaling pathways that promote cancer cell survival (review). Int J Oncol 45:1813–1819CrossRef

46.

Wang X, McCullough KD, Franke TF, Holbrook NJ (2000) Epidermal growth factor receptor dependent Akt activation by oxidative stress enhances cell survival. J BiolChem 275:14624–14631

Title: Photobiomodulation increases cell viability via AKT activation in an in vitro model of diabetes induced by glucose neurotoxicity
Authors: Victória Regina da Silva Oliveira
Rosangela Aparecida Santos-Eichler
Camila Squarzoni Dale
Publication date: 01-02-2020
Publisher: Springer London
Keyword: Laser
Published in: Lasers in Medical Science / Issue 1/2020
Print ISSN: 0268-8921
Electronic ISSN: 1435-604X
DOI: https://doi.org/10.1007/s10103-019-02808-2

At a glance: The STEP trials

Springer Medicine

Photobiomodulation increases cell viability via AKT activation in an in vitro model of diabetes induced by glucose neurotoxicity

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2020

The impact of photobiomodulation of major salivary glands on caries risk

Intravaginal energy-based devices and sexual health of female cancer survivors: a systematic review and meta-analysis

Recalcitrant viral warts treated with photodynamic therapy methyl aminolevulinate and red light (630 nm): a case series of 51 patients

Photobiomodulation therapy at different wavelength impacts on retinoid acid–dependent SH-SY5Y differentiation

Correction to: Effect of 650-nm low-level laser irradiation on c-Jun, c-Fos, ICAM-1, and CCL2 expression in experimental periodontitis

Correction to: Long-term effect of high-intensity laser therapy in the treatment of patients with chronic low back pain: a randomized blinded placebo-controlled trial