Abstract
The impact of mobile phone (MP) radiation on the brain is of specific interest to the scientific community and warrants investigations, as MP is held close to the head. Studies on humans and rodents revealed hazards MP radiation associated such as brain tumors, impairment in cognition, hearing etc. Melatonin (MT) is an important modulator of CNS functioning and is a neural antioxidant hormone. Zebrafish has emerged as a popular model organism for CNS studies. Herein, we evaluated the impact of GSM900MP (GSM900MP) radiation exposure daily for 1 hr for 14 days with the SAR of 1.34 W/Kg on neurobehavioral and oxidative stress parameters in zebrafish. Our study revealed that, GSM900MP radiation exposure, significantly decreased time spent near social stimulus zone and increased total distance travelled, in social interaction test. In the novel tank dive test, the GSM900MP radiation exposure elicited anxiety as revealed by significantly increased time spent in bottom half; freezing bouts and duration and decreased distance travelled, average velocity, and number of entries to upper half of the tank. Exposed zebrafish spent less time in the novel arm of the Y-Maze, corroborating significant impairment in learning as compared to the control group. Exposure decreased superoxide dismutase (SOD), catalase (CAT) activities whereas, increased levels of reduced glutathione (GSH) and lipid peroxidation (LPO) was encountered showing compromised antioxidant defense. Treatment with MT significantly reversed the above neurobehavioral and oxidative derangements induced by GSM900MP radiation exposure. This study traced GSM900MP radiation exposure induced neurobehavioral aberrations and alterations in brain oxidative status. Furthermore, MT proved to be a promising therapeutic candidate in ameliorating such outcomes in zebrafish.
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Sivani, S. and Sudarsanam, D. (2012) Impacts of radio-frequency electromagnetic field (RF-EMF) from cell phone towers and wireless devices on biosystems and ecosystem –a review. Bio. Med., 4, 202–216.
Kumar, N. and Kumar, G. (2009) Biological effects of cell tower radiation on human body, ISMOT, New Delhi, pp. 1365–1368.
Kesari, K.K., Siddiqui, M.H., Meena, R., Verma, H.N. and Kumar, S. (2013) Cell phone radiation exposure on brain and associated biological systems. Indian J. Exp. Biol., 15, 187–200.
Valberg, P.A., van Deventer, T.E. and Repacholi, M.H. (2007) Workgroup report: Base stations and wireless networks: Radiofrequency (RF) exposures and health consequences. Environ. Health Perspect., 115, 416–424.
Repacholi, M.H. (2001) Health risks from the use of mobile phones. Toxicol. Lett., 120, 323–331.
Hamada, A.J., Singh, A. and Agarwal, A. (2011) Cell phones and their impact on male fertility: fact or fiction. Open Reprod. Sci. J., 5, 125–137.
Hardell, L., Carlberg, M. and Hansson Mild, K. (2009) Epide-miological evidence for an association between use of wireless phones and tumor diseases. Pathophysiology, 16, 113–122.
Leszczynski, D., Joenväärä, S., Reivinen, J. and Kuokka, R. (2002) Non-thermal activation of the hsp27/p38MAPK stress pathway by mobile phone radiation in human endothelial cells: molecular mechanism for cancer- and blood-brain barrier related effects. Differentiation, 70, 120–129.
World Health Organization (2007) Neurodegenerative disorders in environmental health criteria. p. 187.
Wilmink, G.J. and Grundt, J.E. (2011) Invited Review Article: Current state of research on biological effects of terahertz radiation. J. Infrared Millim. Terahertz Waves, 32, 1074–1122.
Nittby, H., Grafström, G., Tian, D., Malmgren, L., Brun, A., Persson, B.R., Salford, L.G. and Eberhardt, J. (2008) Cognitive impairment in rats after long-term exposure to GSM–900 mobile phone radiation. Bioelectromagnetics, 29, 219–232.
Narayanan, S.N., Kumar, R.S., Potu, B.K., Nayak, S. and Mailankot, M. (2009) Spatial memory performance of Wistar rats exposed to mobile phone. Clinics (Sao Paulo), 64, 231–234.
Frey, A.H. (1988) Evolution and results of biological research with low-intensity non-ionizing radiation in modern bioelectricity (Marino, A.A. Ed.). Dekker, New York, pp. 785–837.
Salford, L.G., Brun, A., Eberhardt, J.L., Malmgren, L. and Persson, B.R. (2003) Nerve cell damage in mammalian brain after exposure to microwaves from GSM mobile phones. Environ. Health Perspect., 111, 881–883.
Baydas, G., Reiter, R.J., Nedzvetskii, V.S., Yaşar, A., Tuzcu, M., Ozveren, F. and Canatan, H. (2003) Melatonin protects the central nervous system of rats against toluene-containing thinner intoxication by reducing reactive gliosis. Toxicol. Lett., 137, 169–174.
Rodriguez, C., Mayo, J.C., Sainz, R.M., Antolín, I., Herrera, F., Martín, V. and Reiter, R.J. (2004) Regulation of antioxidant enzymes: a significant role for melatonin. J. Pineal Res., 36, 1–9.
Baydas, G., Ozveren, F., Akdemir, I., Tuzcu, M. and Yasar, A. (2005) Learning and memory deficits in rats induced by chronic thinner exposure are reversed by melatonin. J. Pineal Res., 39, 50–56.
Gitto, E., Pellegrino, S., Gitto, P., Barberi, I. and Reiter, R.J. (2009) Oxidative stress of the newborn in the pre- and postnatal period and the clinical utility of melatonin. J. Pineal Res., 46, 128–139.
Korkmaz, A., Reiter, R.J., Topal, T., Manchester, L.C., Oter, S. and Tan, D.X. (2009) Melatonin: an established antioxidant worthy of use in clinical trials. Mol. Med., 15, 43–50.
Menendez-Pelaez, A., Poeggeler, B., Reiter, R.J., Barlow-Walden, L., Pablos, M.I. and Tan, D.X. (1993) Nuclear localization of melatonin in different mammalian tissues: immuno-cytochemical and radioimmunoassay evidence. J. Cell. Biochem., 53, 373–382.
Antolín, I., Rodríguez, C., Saínz, R.M., Mayo, J.C., Uría, H., Kotler, M.L., Rodríguez-Colunga, M.J., Tolivia, D. and Menéndez-Peláez, A. (1996) Neurohormone melatonin prevents cell damage: effect on gene expression for antioxidant enzymes. FASEB J., 10, 882–890.
Barlow-Walden, L.R., Reiter, R.J., Abe, M., Pablos, M., Menendez-Pelaez, A., Chen, L.D. and Poeggeler, B. (1995) Melatonin stimulates brain glutathione peroxidase activity. Neurochem. Int., 26, 497–502.
Melchiorri, D., Reiter, R.J., Attia, A.M., Hara, M., Burgos, A. and Nistico, G. (1995) Potent protective effect of melatonin on in vivo paraquat-induced oxidative damage in rats. Life Sci., 56, 83–89.
Reiter, R., Tang, L., Garcia, J.J. and Muñoz-Hoyos, A. (1997) Pharmacological actions of melatonin in oxygen radical pathophysiology. Life Sci., 60, 2255–2271.
Hardeland, R., Tan, D.X. and Reiter, R.J. (2009) Kynuramines, metabolites of melatonin and other indoles: the resurrection of an almost forgotten class of biogenic amines. J. Pineal Res., 47, 109–126.
Lamb, E.A., Echevarria, D.J. and Jouandot, D.J. (2012) The utility of the T-maze in assessing learning, memory and models of neurological disorders in the zebrafish. Behaviour, 149, 1081–1097.
Guo, S. (2004) Linking genes to brain, behavior, and neurological diseases: What can we learn from zebrafish? Genes Brain Behav., 3, 63–74.
Zhdanova, I.V., Yu, L., Lopez-Patino, M., Shang, E., Kishi, S. and Guelin, E. (2008) Aging of the circadian system in zebrafish and the effects of melatonin on sleep and cognitive performance. Brain Res. Bull., 75, 433–441.
Cognato, G.P., Bortolotto, J.W., Blazina, A.R., Christoff, R.R., Lara, D.R., Vianna, M.R. and Bonan, C.D. (2012) Y-Maze memory task in zebrafish (Danio rerio): The role of glutamatergic and cholinergic systems on the acquisition and consolidation periods. Neurobiol. Learn. Mem., 98, 321–328.
Hall, C.S. (1934) Emotional behavior in the rat. I. Defecation and urination as measures of individual differences in emotionality. J. Com. Psychol., 18, 385–403.
Christmas, A.J. and Maxwell, D.R. (1970) A comparison of the effects of some benzodiazepines and other drugs on aggressive and exploratory behaviour in mice and rats. Neuropharmacology, 9, 17–29.
Prut, L. and Belzung, C. (2003) The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur. J. Pharmacol., 463, 3–33.
Egan, R.J., Bergner, C.L., Hart, P.C., Cachat, J.M., Canavello, P.R., Elegante, M.F., Elkhayat, S.I., Bartels, B.K., Tien, A.K., Tien, D.H., Mohnot, S., Beeson, E., Glasgow, E., Amri, H., Zukowska, Z. and Kalueff, A.V. (2009) Understanding behavioral and physiological phenotypes of stress and anxiety in zebrafish. Behav. Brain Res., 205, 38–44.
Levin, E.D., Bencan, Z. and Cerutti, D.T. (2007) Anxiolytic effects of nicotine in zebrafish. Physiol. Behav., 90, 54–58.
Bencan, Z., Sledge, D. and Levin, E.D. (2009) Buspirone, chlordiazepoxide and diazepam effects in a zebrafish model of anxiety. Pharmacol. Biochem. Behav., 94, 75–80.
Stewart, A., Cachat, J., Wong, K., Gaikwad, S., Gilder, T., DiLeo, J., Chang, K., Utterback, E. and Kalueff, A.V. (2010) Homebase behavior of zebrafish in novelty-based paradigms. Behav. Processes, 85, 198–203.
Grossman, L., Utterback, E., Stewart, A., Gaikwad, S., Chung, K.M., Suciu, C., Wong, K., Elegante, M., Elkhayat, S., Tan, J., Gilder, T., Wu, N., Dileo, J., Cachat, J. and Kalueff, A.V. (2010) Charactrisation of behavioural and endocrine effects of LSD on zebrafish. Behav. Brain Res., 214, 277–84.
Ohkawa, H., Ohishi, N. and Yagi, K. (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem., 95, 351–358.
Sedlak, J. and Lindsay, R.H. (1968) Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal. Biochem., 25, 192–205.
Beers, R.F. Jr. and Sizer, I.W. (1952) A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J. Biol. Chem., 195, 133–140.
Sun, M. and Zigman, S. (1978) An improved spectrophotometric assay for superoxide dismutase based on epinephrine autoxidation. Anal. Biochem., 90, 81–89.
International Telecommunications Union (2010) The world in 2010: ICT facts and figures. Available from: http://www.itu.int/ITU-D/ict/material/FactsFigures2010.pdf.
Kesari, K.K., Kumar, S. and Behari, J. (2010) Mobile phone usage and male infertility in Wistar rats. Indian J. Exp. Biol., 48, 987–992.
Dasdag, S., Akdag, M.Z., Kizil, G., Kizil, M., Cakir, D.U. and Yokus, B. (2012) Effect of 900 MHz radio frequency radiation on beta amyloid protein, protein carbonyl, and malondialdehyde in the brain. Electromagn. Biol. Med., 31, 67–74.
Finnie, J.W., Cai, Z., Manavis, J., Helps, S. and Blumbergs, P.C. (2010) Microglial activation as a measure of stress in mouse brains exposed acutely (60 minutes) and long-term (2 years) to mobile telephone radiofrequency fields. Pathology, 42, 151–154.
Collier, A.D. and Echevarria, D.J. (2013) The utility of the zebrafish model in conditioned place preference to assess the rewarding effects of drugs. Behav. Pharmacol., 24, 375–383.
Iturriaga-Vásquez, P., Osorio, F., Riquelme, S., Catro, S. and Herzog, R. (2012) Zebrafish: A model for behavioural pharmacology. Rev. Farmacol. Chile, 5, 27–32.
Oliveira, R.F. (2013) Mind the fish: zebrafish as a model in cognitive social neuroscience. Front. Neural Circuits, 7, 131.
Bencan, Z. and Levin, E.D. (2008) The role of α7 and α4β2 nicotinic receptors in the nicotine-induced anxiolytic effect in zebrafish. Physiol. Behav., 95, 408–412.
Braida, D., Limonta, V., Pegorini, S., Zani, A., Guerini-Rocco, C., Gori, E. and Sala, M. (2007) Hallucinatory and rewarding effect of salvinorin A in zebrafish: κ-opioid and CB1-cannabinoid receptor involvement. Psychopharmacology, 190, 441–448.
López Patiño, M.A., Yu, L., Yamamoto, B.K. and Zhdanova, I.V. (2008) Gender differences in zebrafish responses to cocaine withdrawal. Physiol. Behav., 95, 36–47.
Bass, S.L. and Gerlai, R. (2008) Zebrafish (Danio rerio) responds differentially to stimulus fish: the effects of sympatric and allopatric predators and harmless fish. Behav. Brain Res., 186, 107–117.
Speedie, N. and Gerlai, R. (2008) Alarm substance induced behavioral responses in zebrafish (Danio rerio). Behav. Brain Res., 188, 168–177.
Stewart, A., Gaikwad, S., Kyzar, E., Green, J., Roth, A. and Kalueff, A. (2012) Modeling anxiety using adult zebrafish: A conceptual review. Neuropharmacology, 62, 135–143.
Daniels, W.M., Pitout, I.L., Afullo, T.J. and Mabandla, M.V. (2009) The effect of electromagnetic radiation in the mobile phone range on the behaviour of the rat. Metab. Brain Dis., 24, 629–641.
Sokolovic, D., Djordjevic, B., Kocic, G., Babovic, P., Ristic, G., Stanojkovic, Z., Sokolovic, D.M., Veljkovic, A., Jankovic, A. and Radovanovic, Z. (2012) The effect of melatonin on body mass and behaviour of rats during an exposure to microwave radiation from mobile phone. Bratisl. Lek. Listy., 113, 265–269.
Haarala, C., Takio, F., Rintee, T., Laine, M., Koivisto, M., Revonsuo, A. and Hämäläinen, H. (2007) Pulsed and continuous wave mobile phone exposure over left versus right hemisphere: effects on human cognitive function. Bioelectromagnetics, 28, 289–295.
Kwon, M.S., Koivisto, M., Laine, M. and Hämäläinen, H. (2008) Perception of the electromagnetic field emitted by a mobile phone. Bioelectromagnetics, 29, 154–159.
Ntzouni, M.P., Stamatakis, A., Stylianopoulou, F. and Margaritis, L.H. (2011) Short-term memory in mice is affected by mobile phone radiation. Pathophysiology, 18, 193–199.
Schrader, S.M. and Kanitz, M.H. (1994) Occupational hazards to male reproduction in occupational medicine: State of the art reviews. (Gold, E., Schenker, M. and Lasley, B. Ed.). Hanley and Belfus, Philadelphia, pp. 405–414.
Rahman, K. (2007) Studies on free radicals, antioxidants, and co-factors. Clin. Interv. Aging, 2, 219–236.
Lillig, C.H., Berndt, C. and Holmgren, A. (2008) Glutaredoxin systems. Biochim. Biophys. Acta, 1780, 1304–1317.
Conterato, G.M., Augusti, P.R., Somacal, S., Einsfeld, L., Sobieski, R., Torres, J.R. and Emaneulli, T. (2007) Effect of lead acetate on cytosolic thioredoxin reductase activity and oxidative stress parameters in rat kidneys. Basic Clin. Pharmacol. Toxicol., 101, 96–100.
Narayanan, P.K., Carter, W.O., Ganey, P.E., Roth, R.A., Voytik-Harbin, S.L. and Robinson, J.P. (1998) Impairment of human neutrophil oxidative burst by polychlorinated biphenyls: inhibition of superoxide dismutase activity. J. Leukoc. Biol., 63, 216–224.
Manda, K., Ueno, M. and Anzai, K. (2008) Space radiation-induced inhibition of neurogenesis in the hippocampal dentate gyrus and memory impairment in mice: ameliorative potential of the melatonin metabolite, AFMK. J. Pineal Res., 45, 430–438.
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Nirwane, A., Sridhar, V. & Majumdar, A. Neurobehavioural Changes and Brain Oxidative Stress Induced by Acute Exposure to GSM900 Mobile Phone Radiations in Zebrafish (Danio rerio). Toxicol Res. 32, 123–132 (2016). https://doi.org/10.5487/TR.2016.32.2.123
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DOI: https://doi.org/10.5487/TR.2016.32.2.123