Activation of liver X receptors ameliorates alterations in testicular function in rats exposed to electromagnetic radiation

References

• Oh JJ, Byun SS, Lee SE, et al. Effect of electromagnetic waves from mobile phones on spermatogenesis in the era of 4G-LTE. Biomed Res Int. 2018;2018:1801798. PMID: 29789776
   Web of Science ®Google Scholar
• Agarwal A, Deepinder F, Sharma RK, et al. Effect of cell phone usage on semen analysis in men attending infertility clinic: an observational study. Fertil Steril. 2008;89(1):124–128. PMID: 17482179
   PubMed Web of Science ®Google Scholar
• Kesari KK, Behari J. Evidence for mobile phone radiation exposure effects on reproductive pattern of male rats: role of ROS. Electromagn Biol Med. 2012;31(3):213–222. PMID: 22897402
   PubMed Web of Science ®Google Scholar
• Bhatt CR, Redmayne M, Abramson MJ, et al. Instruments to assess and measure personal and environmental radiofrequency-electromagnetic field exposures. Australas Phys Eng Sci Med. 2016;39(1):29–42. PMID: 26684750
   Web of Science ®Google Scholar
• Liu K, Li Y, Zhang G, et al. Association between mobile phone use and semen quality: a systemic review and meta-analysis. Andrology. 2014;2(4):491–501. PMID: 24700791
   Web of Science ®Google Scholar
• Wdowiak A, Wdowiak L, Wiktor H. Evaluation of the effect of using mobile phones on male fertility. Ann Agric Environ Med. 2007;14(1): 169–172. PMID: 17655195.
   PubMed Web of Science ®Google Scholar
• Çetkin M, Kızılkan N, Demirel C, et al. Quantitative changes in testicular structure and function in rat exposed to mobile phone radiation. Andrologia. 2017;49(10):e12761. PMID: 28124386
   Web of Science ®Google Scholar
• Amara S, Abdelmelek H, Garrel C, et al. Effects of subchronic exposure to static magnetic field on testicular function in rats. Arch Med Res. 2006;37(8):947–952. PMID: 17045109
   Web of Science ®Google Scholar
• Pandey N, Giri S. Melatonin attenuates radiofrequency radiation (900 MHz)-induced oxidative stress, DNA damage and cell cycle arrest in germ cells of male Swiss albino mice. Toxicol Ind Health. 2018;34(5):315–327. PMID: 29562845
   PubMed Web of Science ®Google Scholar
• Kim SJ, Jang YW, Hyung KE, et al. Extremely low-frequency electromagnetic field exposure enhances inflammatory response and inhibits effect of antioxidant in RAW 264.7 cells. Bioelectromagnetics. 2017;38(5):374–385. PMID: 28370033
   Web of Science ®Google Scholar
• Mahaki H, Tanzadehpanah H, Jabarivasal N, et al. A review on the effects of extremely low frequency electromagnetic field (ELF-EMF) on cytokines of innate and adaptive immunity. Electromagn Biol Med. 2019;38(1):84–95. PMID: 30518268
   PubMed Web of Science ®Google Scholar
• Komati R, Spadoni D, Zheng S, et al. Ligands of therapeutic utility for the liver X receptors. version 2. Molecules. 2017;2(1):88–111. PMID: 28067791 .
   Google Scholar
• Makker K, Agarwal A, Sharma R. Oxidative stress & male infertility. Indian J Med Res. 2009;129(4): 357–367. PMID: 19535829.
   PubMed Web of Science ®Google Scholar
• Volle DH, Mouzat K, Duggavathi R, et al. Multiple roles of the nuclear receptors for oxysterols liver X receptor to maintain male fertility. Mol Endocrinol. 2007;21(5):1014–1027. PMID: 17341595
   Google Scholar
• Rondanino C, Ouchchane L, Chauffour C, et al. Levels of liver X receptors in testicular biopsies of patients with azoospermia. Fertil Steril. 2014;102(2):361–71.e5. PMID: 24842676
   PubMed Web of Science ®Google Scholar
• Fessler MB. The challenges and promise of targeting the liver X receptors for treatment of inflammatory disease. Pharmacol Ther. 2018;181:1–12. PMID: 28720427.
   PubMed Web of Science ®Google Scholar
• El-Maleky NF, Ebrahim RH. Effects of exposure to electromagnetic field from mobile phone on serum hepcidin and iron status in male albino rats. Electromagn Biol Med. 2019;38(1):66–73. PMID: 30388901 .
   PubMed Web of Science ®Google Scholar
• Tachibana H, Ogawa D, Matsushita Y, et al. Activation of liver X receptor inhibits osteopontin and ameliorates diabetic nephropathy. J Am Soc Nephrol. 2012;23(11):1835–1846. PMID: 23085633 .
   Web of Science ®Google Scholar
• Bahaodini A, Owjfard M, Tamadon A, et al. Low frequency electromagnetic fields long-term exposure effects on testicular histology, sperm quality and testosterone levels of male rats. Asian Pac J Reprod. 2015;4(3):195–200.
   Google Scholar
• Mailankot M, Kunnath AP, Jayalekshmi H, et al. Radio frequency electromagnetic radiation (RF-EMR) from GSM (0.9/1.8GHz) mobile phones induces oxidative stress and reduces sperm motility in rats. Clinics (Sao Paulo). 2009;64(6):561–565. PMID: 19578660
   PubMed Web of Science ®Google Scholar
• Gautam R, Singh KV, Nirala J, et al. Oxidative stress-mediated alterations on sperm parameters in male wistar rats exposed to 3G mobile phone radiation. Andrologia. 2019;51(3):e13201. PMID: 30461041
   PubMed Web of Science ®Google Scholar
• Okechukwu CE. Effects of mobile phone radiation and exercise on testicular function in male wistar rats. Niger J Exp Clin Biosci. 2018;6(2):51–58.
   Google Scholar
• Tumkaya L, Kalkan Y, Bas O, et al. Mobile phone radiation during pubertal development has no effect on testicular histology in rats. Toxicol Ind Health. 2016;32(2):328–336. PMID: 24097363
   PubMed Web of Science ®Google Scholar
• Toocheck C, Clister T, Shupe J, et al. Mouse spermatogenesis requires classical and nonclassical testosterone signaling. Biol Reprod. 2016;94(1):11–24. PMID: 26607719
   Web of Science ®Google Scholar
• Jarvis S, Williamson C, Bevan CL. Liver X Receptors and Male (In) fertility. Int J Mol Sci. 2019;20(21):5379–5392. PMID: 31671745 .
   Web of Science ®Google Scholar
• Oyewopo AO, Olaniyi SK, Oyewopo CI, et al. Radiofrequency electromagnetic radiation from cell phone causes defective testicular function in male wistar rats. Andrologia. 2017;49(10):e12772. PMID: 28261838
   Web of Science ®Google Scholar
• Meo SA, Al-Drees AM, Husain S, et al. Effects of mobile phone radiation on serum testosterone in wistar albino rats. Saudi Med J. 2010;31(8): 869–873. PMID: 20714683.
   PubMed Web of Science ®Google Scholar
• Sepehrimanesh M, Saeb M, Nazifi S, et al. Impact of 900 MHz electromagnetic field exposure on main male reproductive hormone levels: a rattus norvegicus model. Int J Biometeorol. 2014;58(7):1657–1663. PMID: 24357488
   Web of Science ®Google Scholar
• Ozguner M, Koyu A, Cesur G, et al. Biological and morphological effects on the reproductive organ of rats after exposure to electromagnetic field. Saudi Med J. 2005;26(3): 405–410. PMID: 15806208.
   PubMed Web of Science ®Google Scholar
• Forgács Z, Somosy Z, Kubinyi G, et al. Effect of whole-body 1800MHz GSM-like microwave exposure on testicular steroidogenesis and histology in mice. Reprod Toxicol. 2006;22(1):111–117. PMID: 16434166
   PubMed Web of Science ®Google Scholar
• Ozlem Nisbet H, Nisbet C, Akar A, et al. Effects of exposure to electromagnetic field (1.8/0.9 GHz) on testicular function and structure in growing rats. Res Vet Sci. 2012;93(2):1001–1005. PMID: 22130559
   Web of Science ®Google Scholar
• Ribeiro EP, Rhoden EL, Horn MM, et al. Effects of subchronic exposure to radio frequency from a conventional cellular telephone on testicular function in adult rats. J Urol. 2007;177(1):395–399. PMID: 17162098
   Web of Science ®Google Scholar
• Agarwal A, Desai NR, Makker K, et al. Effects of radiofrequency electromagnetic waves (RF-EMW) from cellular phones on human ejaculated semen: an in vitro pilot study. Fertil Steril. 2009;92(4):1318–1325. PMID: 18804757.
   PubMed Web of Science ®Google Scholar
• Dasdag S, Zulkuf Akdag M, Aksen F, et al. Whole body exposure of rats to microwaves emitted from a cell phone does not affect the testes. Bioelectromagnetics. 2003;24(3):182–188. PMID: 12669301
   Web of Science ®Google Scholar
• Falzone N, Huyser C, Franken DR, et al. Mobile phone radiation does not induce pro-apoptosis effects in human spermatozoa. Radiat Res. 2010 Aug;174(2):169–176. PMID: 20681783.
   Web of Science ®Google Scholar
• Hichor M, Sundaram VK, Eid SA, et al. Liver X receptor exerts a protective effect against the oxidative stress in the peripheral nerve. Sci Rep. 2018;8(1):2524–2536. PMID: 29410501
   Google Scholar
• He Q, Pu J, Yuan A, et al. Activation of liver-X-receptor α but not liver-X-receptor β protects against myocardial ischemia/reperfusion injury. Circ Heart Fail. 2014;7(6):1032–1041. PMID: 25277999
   Web of Science ®Google Scholar
• Patel M, Wang XX, Magomedova L, et al. Liver X receptors preserve renal glomerular integrity under normoglycaemia and in diabetes in mice. Diabetologia. 2014;57(2):435–446. PMID: 24201575
   Web of Science ®Google Scholar
• Heeba GH, Mahmoud ME. Therapeutic potential of morin against liver fibrosis in rats: modulation of oxidative stress, cytokine production and nuclear factor kappa B. Environ Toxicol Pharmacol. 2014;37(2):662–671. PMID: 24583409
   PubMed Web of Science ®Google Scholar
• Prahalathan P, Kumar S, Raja B. Morin attenuates blood pressure and oxidative stress in deoxycorticosterone acetate-salt hypertensive rats: a biochemical and histopathological evaluation. Metabolism. 2012;61(8):1087–1099. PMID: 22386933
   Web of Science ®Google Scholar
• Pall ML. Electromagnetic fields act via activation of voltage-gated calcium channels to produce beneficial or adverse effects. J Cell Mol Med. 2013;17(8):958–965. PMID: 23802593
   PubMed Web of Science ®Google Scholar
• Hosseinabadi MB, Khanjani N, Samaei SE, et al. Effect of long-term occupational exposure to extremely low- frequency electromagnetic fields on pro-inflammatory cytokine and hematological parameters. Int J Radiat Biol. 2019;95(11):1573–1580. PMID: 31329007
   PubMed Web of Science ®Google Scholar
• Zhang D, Zhang Y, Zhu B, et al. Resveratrol may reverse the effects of long-term occupational exposure to electromagnetic fields on workers of a power plant. Oncotarget. 2017;8(29):47497–47506. PMID: 28537898
   Google Scholar
• Wang Z, Fei Y, Liu H, et al. Effects of electromagnetic fields exposure on plasma hormonal and inflammatory pathway biomarkers in male workers of a power plant. Int Arch Occup Environ Health. 2016;89(1):33–42. PMID: 25808749
   Web of Science ®Google Scholar
• Bhushan S, Tchatalbachev S, Lu Y, et al. Differential activation of inflammatory pathways in testicular macrophages provides a rationale for their subdued inflammatory capacity. J Immunol. 2015;194(11):5455–5464. PMID: 25917085
   Web of Science ®Google Scholar
• Ott M, Gogvadze V, Orrenius S, et al. Mitochondria, oxidative stress and cell death. Apoptosis. 2007;12(5):913–922. PMID: 17453160
   PubMed Web of Science ®Google Scholar
• Sinha K, Das J, Pal PB, et al. Oxidative stress: the mitochondria-dependent and mitochondria-independent pathways of apoptosis. Arch Toxicol. 2013;87(7):1157–1180. PMID: 23543009
   PubMed Web of Science ®Google Scholar
• McIlwain DR, Berger T, Mak TW. Caspase functions in cell death and disease. Cold Spring Harb Perspect Biol. 2013;5(4):a008656. PMID: 23545416
   PubMed Web of Science ®Google Scholar
• Liu Q, Si T, Xu X, et al. Electromagnetic radiation at 900 MHz induces sperm apoptosis through bcl-2, bax and caspase-3 signaling pathways in rats. Reprod Health. 2015;12:65–73. PMID: 26239320.
   PubMed Web of Science ®Google Scholar
• Falzone N, Huyser C, Franken DR, et al. Mobile phone radiation does not induce pro-apoptosis effects in human spermatozoa. Radiat Res. 2010;174(2):169–176. PMID: 20681783
   Web of Science ®Google Scholar
• Tas M, Dasdag S, Akdag MZ, et al. Long-term effects of 900 MHz radiofrequency radiation emitted from mobile phone on testicular tissue and epididymal semen quality. Electromagn Biol Med. 2014;33(3):216–222. PMID: 23781998
   PubMed Web of Science ®Google Scholar
• Trošić I, Mataušić-Pišl M, Pavičić I, et al. Histological and cytological examination of rat reproductive tissue after short-time intermittent radiofrequency exposure. Arh Hig Rada Toksikol. 2013;64(4):513–519. PMID: 24384757
   Web of Science ®Google Scholar