Evaluation of Aquaporins 1 and 5 Expression in Rat Parotid Glands After Volumetric Modulated Arc Radiotherapy and Use of Low-Level Laser Therapy at Different Times
Journal of Lasers in Medical Sciences,
Vol. 11 No. 3 (2020),
21 June 2020
,
Page 262-267
Abstract
Introduction: This experimental study investigated the mRNA expression of aquaporins (AQPs) 1 and 5 in the parotid glands of rats irradiated with volumetric modulated arc therapy (VMAT) and subjected to low-level laser therapy (LLLT) at different time points.
Methods: The sample consisted of 30 Wistar rats (Rattus norvegicus) divided into the following groups: control, LLLT alone (LG), radiotherapy alone (RG), and experimental groups that received LLLT at 24 hours (early experimental group [EEG], n=12) and 120 hours (late experimental group [LEG], n=12) after radiotherapy. VMAT was delivered at a single dose (12 Gy) and LLLT was performed with an aluminium-gallium-arsenide diode laser (660 nm, 100 mW), spot area of 0.0028 cm2, energy of 2 J/cm2 applied to 3 spots in the region corresponding to the right parotid gland, for 10 consecutive days. The right parotid gland was resected and prepared for RNA extraction. The gene expression of AQPs was evaluated by quantitative polymerase chain reaction (qPCR) using specific TaqMan probes, with the HPRT gene as an internal control.
Results: The lowest AQP1 gene expression was 0.83 (0.27) with the use of LLLT 24 hours after radiotherapy (EEG), and the highest was 1.56 (0.80) with the use of LLLT alone (LG). Likewise, the lowest AQP5 gene expression was found in the EEG (mean = 0.88; SD = 0.49) and the highest in the LG (mean = 1.29; SD = 0.33).
Conclusion: The use of LLLT after radiotherapy may contribute to the maintenance and an increase of these proteins, even when used at a later time point after radiotherapy.
- Aquaporins
- Salivary glands
- Intensity-modulated radiotherapy
- Low-level light therapy
- Rats.
How to Cite
References
Saleh J, Figueiredo MA, Cherubini K, Salum FG. Salivary hypofunction: An update on aetiology, diagnosis and therapeutics. Arch Oral Biol. 2014;60(2):242-255. doi: 10.1016/j.archoralbio.2014.10.004.
Bahl A, Oinam AS, Kaur S, Verma R, Elangovan A, Bhandari S, et al. Evaluation of acute toxicity and early clinical outcome in head and neck cancers treated with conventional radiotherapy and simultaneous integrated boost arc radiotherapy. World J Oncol. 2017;8(5):174. doi: 10.14740/wjon1049wc1.
Vissink A, Jansma J, Spijkervet FK, Burlage FR, Coppes RP. Prevention and Treatment of the Consequences of Head and Neck Radiotherapy. Crit Rev Oral Biol Med. 2003;14(3):199-212. doi: 10.1177/154411130301400305
Freitas DA, Caballero AD, Pereira MM, Oliveira SK, Silva GP, Hernández CI. Oral sequelae of head and neck radiotherapy. Rev CEFAC. 2011;13(6):1103-1108. doi: 10.1590/s1516-18462011005000071.
Baum BJ, Zheng C, Cotrim AP, Goldsmith CM, Atkinson JC, Brahim JS, et al. Transfer of the AQP1 cDNA for the correction of radiation-induced salivary hypofunction. Biochim Biophys Acta Biomembr. 2006;1758(8):1071-1077. doi: 10.1016/j.bbamem.2005.11.006.
Lee SW, Kang KW, Wu HG. Prospective investigation and literature review of tolerance dose on salivary glands using quantitative salivary gland scintigraphy in the intensity-modulated radiotherapy era. Head Neck. 2016;38(Suppl 1):E1746-55. doi: 10.1002/hed.24310.
Van Gestel D, Van Den Weyngaert D, Schrijvers D, Weyler J, Vermorken JB. Intensity-modulated radiotherapy in patients with head and neck cancer: A European single-centre experience. Br J Radiol. 2011;84(1000), 367-374. doi: 10.1259/bjr/67058055.
França CM, França CM, Núñez SC, Prates RA, Noborikawa E, Faria MR, et al. Low-intensity red laser on the prevention and treatment of induced-oral mucositis in hamsters. J Photochem Photobiol B. 2009;94(1):25-31. doi: 10.1016/j.jphotobiol.2008.09.006.
González-Arriagada WA, Ramos LMA, Andrade MAC, Lopes MA. Efficacy of low-level laser therapy as an auxiliary tool for management of acute side effects of head and neck radiotherapy. J Cosmet Laser Ther. 2018;20(2):117-122. doi: 10.1080/14764172.2017.1376097.
Lončar B, Stipetić MM, Baričević M, Risović D. The effect of low-level laser therapy on salivary glands in patients with xerostomia. Photomed Laser Surg. 2011;29(3):171-175. doi: 10.1089/pho.2010.2792.
Basirat M. The effects of low power lasers in healing of oral ulcers. J Lasers Med Sci. 2012;3(2):79-83. doi: 10.22037/jlms.v3i2.3209.
Fekrazad R, Chiniforush N. Oral mucositis prevention and management by therapeutic laser in head and neck cancers. J Lasers Med Sci. 2014;5(1):1-7. doi:10.22037/jlms.v5i1.5460.
Acauan MD, Gomes AP, Braga-Filho A, de Figueiredo MA, Cherubini K, Salum FG. Effect of low-level laser therapy on irradiated parotid glands—study in mice. J Biomed Opt. 2015; 20(10):108002. doi: 10.1117/1.jbo.20.10.108002.
Gonnelli FA, Palma LF, Giordani AJ, Deboni AL, Dias RS, Segreto RA, et al. Low-level laser therapy for the prevention of low salivary flow rate after radiotherapy and chemotherapy in patients with head and neck cancer. Radiol Bras. 2016;49(2):86-91. doi: 10.1590/0100-3984.2014.0144.
Plavnik LM, De Crosa ME, Malberti AI. Effect of low-power radiation (Helium/Neon) upon submandibulary glands. J Clin Laser Med Surg. 2003;21(4):219-225. doi: 10.1089/104454703768247792.
Saleh J, Figueiredo MA, Cherubini K, Braga-Filho A, Salum FG. Effect of low-level laser therapy on radiotherapy-induced hyposalivation and xerostomia: A pilot study. Photomed Laser Surg. 2014;32(10):546-552. doi: 10.1089/pho.2014.3741.
Vidović Juras D, Lukač J, Cekić-Arambašin A, Vidović A, Canjuga I, Sikora M, et al. Effects of low-level laser treatment on mouth dryness. Coll Antropol. 2010;34(3):1039-43.
Benga G. Water channel proteins (later called aquaporins) and relatives: Past, present, and future. IUBMB Life. 2009;61(2):112-33. doi: 10.1002/iub.156.
Delporte C, Steinfeld S. Distribution and roles of aquaporins in salivary glands. Biochim Biophys Acta Biomembr. 2006;1758(8):1061-70. doi: 10.1016/j.bbamem.2006.01.022.
Delporte C, Bryla A, Perret J. Aquaporins in salivary glands: From basic research to clinical applications. Int J Mol Sci. 2016;17(2):166. doi: 10.3390/ijms17020166.
Aure MH, Ruus AK, Galtung HK. Aquaporins in the adult mouse submandibular and sublingual salivary glands. J Mol Histol. 2014;45(1):69-80. doi: 10.1007/s10735-013-9526-3.
Hosoi K. Physiological role of aquaporin 5 in salivary glands. Pflugers Arch. 2016;468(4):519-39. doi: 10.1007/s00424-015-1749-6.
Ishikawa Y, Cho G, Yuan Z, Inoue N, Nakae Y. Aquaporin-5 water channel in lipid rafts of rat parotid glands. Biochim Biophys Acta Biomembr. 2006;1758(8):1053-60. doi: 10.1016/j.bbamem.2006.03.026.
Piva JA, Abreu EM, Silva Vdos S, Nicolau RA. Effect of low-level laser therapy on the initial stages of tissue repair: basic principles. An Bras Dermatol. 2011;86(5), 947–954. doi: 10.1590/s0365-05962011000500013.
Li Z, Zhao D, Gong B, Xu Y, Sun H, Yang B, et al. Decreased saliva secretion and down-regulation of AQP5 in submandibular gland in irradiated rats. Radiat Res. 2006;165(6):678-687. doi: 10.1667/rr3569.1.
Larsen HS, Ruus AK, Galtung HK. Aquaporin expression patterns in the developing mouse salivary gland. Eur J Oral Sci. 2009;117(6):655–662. doi: 10.1111/j.1600-0722.2009.00695.x.
Bjordal JM, Bensadoun RJ, Tunèr J, Frigo L, Gjerde K, Lopes-Martins RA. A systematic review with meta-analysis of the effect of low-level laser therapy (LLLT) in cancer therapy-induced oral mucositis. Support Care Cancer. 2011;19(8):1069-77. doi: 10.1007/s00520-011-1202-0.
Boom R, Sol CJ, Salimans MM, Jansen CL, Wertheim-Van Dillen PM, van der Noordaa J. Rapid and simple method for purification of nucleic acids. J Clin Microbiol. 1990;28(3):495-503.
Bomfim FRC, Sella VRG, Thomasini RL, Plapler H. Influence of low-level laser irradiation on osteocalcin protein and gene expression in bone tissue1. Acta Cir Bras. 2018;33(9):736-743. doi: 10.1590/s0102-865020180090000001.
Sugimoto N, Matsuzaki K, Ishibashi H, Tanaka M, Sawaki T, Fujita Y, et al. Upregulation of aquaporin expression in the salivary glands of heat-acclimated rats. Sci Rep. 2013;3:1763. doi: 10.1038/srep01763.
Araujo MVT, Spadella MA, Chies AB, Arruda GV, Santos TM, Cavariani MM, et al. Effect of low radiation dose on the expression and location of aquaporins in rat submandibular gland. Tissue Cell. 2018;53:104-110. doi: 10.1016/j.tice.2018.06.006.
de Paula F, Teshima THN, Hsieh R, Souza MM, Coutinho-Camillo CM, Nico MMS, et al. The expression of water channel proteins during human salivary gland development: a topographic study of aquaporins 1, 3 and 5. J Mol Histol. 2017; 48(5):329-336. doi: 10.1007/s10735-017-9731-6.
Simões A, Siqueira WL, Lamers ML, Santos MF, Eduardo Cde P, Nicolau J. Laser phototherapy effect on protein metabolism parameters of rat salivary glands. Lasers Med Sci. 2009;24(2):202-208. doi: 10.1007/s10103-008-0548-0.
Pan Y, Iwata F, Wang D, Muraguchi M, Ooga K, Ohmoto Y, et al. Identification of aquaporin-5 and lipid rafts in human resting saliva and their release into cevimeline-stimulated saliva. Biochim Biophys Acta Gen Subj. 2009;1790(1):49-56. doi: 10.1016/j.bbagen.2008.08.009.
Karu TI. Multiple roles of cytochrome c oxidase in mammalian cells under action of red and IR-A radiation. IUBMB Life. 2010;62(8):607-10. doi: 10.1002/iub.359
Zecha JA, Raber-Durlacher JE, Nair RG, Epstein JB, Elad S, Hamblin MR, et al. Low-level laser therapy/photobiomodulation in the management of side effects of chemoradiation therapy in head and neck cancer: part 2: proposed applications and treatment protocols. Support Care Cancer. 2016;24(6):2793-2805. doi: 10.1007/s00520-016-3153-y.
de Freitas LF, Hamblin MR. Proposed Mechanisms of Photobiomodulation or Low-Level Light Therapy. IEEE J Sel Top Quantum Electron. 2016;22(3). doi: 10.1109/JSTQE.2016.2561201.
Lins RD, Dantas EM, Lucena KC, Catão MH, Granville-Garcia AF, Carvalho Neto LG. Biostimulatory effects of low power laser in the repair process. An Bras Dermatol. 2010;85(6):849-55. doi: 10.1590/S0365-05962010000600011.
Gresz V, Burghardt B, Ferguson CJ, Hurley PT, Takács M, Nielsen S, et al. Expression of aquaporin 1 (AQP1) water channels in human labial salivary glands. Arch Oral Biol. 1999;44(Suppl 1):S53-S7. doi: 10.1016/S0003-9969(99)90020-1.
Gresz V, Kwon TH, Gong H, Agre P, Steward MC, King LS, et al. Immunolocalization of AQP-5 in rat parotid and submandibular salivary glands after stimulation or inhibition of secretion in vivo. Am J Physiol Gastrointest Liver Physiol. 2004;287(1):G151-61. doi: 10.1152/ajpgi.00480.2003.
Tatsuishi Y, Hirota M, Kishi T, Adachi M, Fukui T, Mitsudo K, et al. Human salivary gland stem/progenitor cells remain dormant even after irradiation. Int J Mol Med. 2009;24(3):361-366. doi: 10.3892/ijmm_00000240.
Gresz V, Horvath A, Gera I, Nielsen S, Zelles T. Immunolocalization of AQP5 in resting and stimulated normal labial glands and in Sjögren’s syndrome. Oral Dis. 2015;21(1):e114-e120. doi: 10.1111/odi.12239.
- Abstract Viewed: 432 times
- PDF Downloaded: 295 times