Exposure to long-term evolution radiofrequency electromagnetic fields decreases neuroblastoma cell proliferation via Akt/mTOR-mediated cellular senescence

References

• Abbas, T., and A. Dutta. 2009. p21 in cancer: Intricate networks and multiple activities. Nat. Rev. Cancer 9:400–14. doi:10.1038/nrc2657.
   PubMed Web of Science ®Google Scholar
• Adams, P. D. 2001. Regulation of the retinoblastoma tumor suppressor protein by cyclin/cdks. BBA-Rev. Cancer 1471:M123–M133.
   PubMed Web of Science ®Google Scholar
• Astle, M. V., K. M. Hannan, P. Y. Ng, R. S. Lee, A. J. George, A. K. Hsu, Y. Haupt, R. D. Hannan, and R. B. Pearson. 2012. AKT induces senescence in human cells via mTORC1 and p53 in the absence of DNA damage: Implications for targeting mTOR during malignancy. Oncogene 31:1949–62. doi:10.1038/onc.2011.394.
   PubMed Web of Science ®Google Scholar
• Baan, R., Y. Grosse, B. Lauby-Secretan, F. El Ghissassi, V. Bouvard, L. Benbrahim-Tallaa, N. Guha, F. Islami, L. Galichet, and K. Straif. 2011. Carcinogenicity of radiofrequency electromagnetic fields. Lancet Oncol. 12:624–26. doi:10.1016/S1470-2045(11)70147-4.
   PubMed Web of Science ®Google Scholar
• Bouji, M., A. Lecomte, C. Gamez, K. Blazy, and A. S. Villégier. 2020. Impact of cerebral radiofrequency exposures on oxidative stress and corticosterone in a rat model of Alzheimer’s disease. J. Alzheimer’s Dis. 73:467–76. doi:10.3233/JAD-190593.
   PubMed Web of Science ®Google Scholar
• Buttiglione, M., L. Roca, E. Montemurno, F. Vitiello, V. Capozzi, and G. Cibelli. 2007. Radiofrequency radiation (900 MHz) induces Egr-1 gene expression and affects cell-cycle control in human neuroblastoma cells. J. Cell. Physiol. 213:759–67. doi:10.1002/jcp.21146.
   PubMed Web of Science ®Google Scholar
• Chiarle, R., M. Pagano, and G. Inghirami. 2000. The cyclin dependent kinase inhibitor p27 and its prognostic role in breast cancer. Breast Cancer Res. 3:91. doi:10.1186/bcr277.
   PubMed Web of Science ®Google Scholar
• Chien, W. W., C. Domenech, R. Catallo, G. Salles, and M. Ffrench. 2010. S-phase lengthening induced by p16(INK4a) overexpression in malignant cells with wild-type pRb and p53. Cell Cycle 9:3286–96. doi:10.4161/cc.9.16.12600.
   PubMed Web of Science ®Google Scholar
• Choi, J., K. Min, S. Jeon, N. Kim, J. K. Pack, and K. Song. 2020. Continuous exposure to 1.7 GHz LTE electromagnetic fields increases intracellular reactive oxygen species to decrease human cell proliferation and induce senescence. Sci. Rep. 10:9238. doi:10.1038/s41598-020-65732-4.
   PubMed Web of Science ®Google Scholar
• Corveloni, A. C., S. C. Semprebon, A. Baranoski, B. I. Biazi, T. A. Zanetti, and M. S. Mantovani. 2020. Carnosic acid exhibits antiproliferative and proapoptotic effects in tumoral NCI-H460 and nontumoral IMR-90 lung cells. J. Toxicol. Environ. Health A 83:412–21. doi:10.1080/15287394.2020.1767741.
   PubMed Web of Science ®Google Scholar
• Gherardini, L., G. Ciuti, S. Tognarelli, and C. Cinti. 2014. Searching for the perfect wave: The effect of radiofrequency electromagnetic fields on cells. Int. J. Mol. Sci. 15:5366–87. doi:10.3390/ijms15045366.
   PubMed Web of Science ®Google Scholar
• Giacinti, C., and A. Giordano. 2006. RB and cell cycle progression. Oncogene 25:5220–27. doi:10.1038/sj.onc.1209615.
   PubMed Web of Science ®Google Scholar
• Goodrich, D. W., N. P. Wang, Y.-W. Qian, E. Y. H. P. Lee, and W.-H. Lee. 1991. The retinoblastoma gene product regulates progression through the G1 phase of the cell cycle. Cell 67:293–302. doi:10.1016/0092-8674(91)90181-W.
   PubMed Web of Science ®Google Scholar
• Houston, B. J., B. Nixon, B. V. King, R. J. Aitken, and G. N. De Iuliis. 2018. Probing the origins of 1,800 MHz radio frequency electromagnetic radiation induced damage in mouse immortalized germ cells and spermatozoa in vitro. Front. Public. Health 6:270. doi:10.3389/fpubh.2018.00270.
   PubMed Web of Science ®Google Scholar
• Houston, B. J., B. Nixon, B. V. King, G. N. De Iuliis, and R. J. Aitken. 2016. The effects of radiofrequency electromagnetic radiation on sperm function. Reproduction 152:R263–R276. doi:10.1530/REP-16-0126.
   PubMed Web of Science ®Google Scholar
• Ishihara, T., K. Yamazaki, A. Araki, Y. Teraoka, N. Tamura, T. Hikage, M. Omiya, M. Mizuta, and R. Kishi. 2020. Exposure to radiofrequency electromagnetic field in the high-frequency band and cognitive function in children and adolescents: A literature review. Int. J. Environ. Res. Public Health 17:9179. doi:10.3390/ijerph17249179.
   Web of Science ®Google Scholar
• Jung, S. H., H. J. Hwang, D. Kang, H. A. Park, H. C. Lee, D. Jeong, K. Y. Lee, H. J. Park, Y.-G. Ko, and J.-S. Lee. 2019. mTOR kinase leads to PTEN-loss-induced cellular senescence by phosphorylating p53. Oncogene 38:1639–50. doi:10.1038/s41388-018-0521-8.
   PubMed Web of Science ®Google Scholar
• Karar, J., and A. Maity. 2011. PI3K/AKT/mTOR pathway in angiogenesis. Front. Mol. Neurosci. 4. doi:10.3389/fnmol.2011.00051.
   PubMedGoogle Scholar
• Kesari, K. K., A. Agarwal, and R. Henkel. 2018. Radiations and male fertility. Reprod. Biol. Endocrinol. 16:1–16. doi:10.1186/s12958-018-0431-1.
   PubMed Web of Science ®Google Scholar
• Kim, J. H., Y. H. Huh, and H. R. Kim. 2016. Induction of autophagy in the striatum and hypothalamus of mice after 835 MHz radiofrequency exposure. PLoS One 11:e0153308. doi:10.1371/journal.pone.0153308.
   PubMed Web of Science ®Google Scholar
• Kim, J. H., C. H. Lee, H. G. Kim, and H. R. Kim. 2019. Decreased dopamine in striatum and difficult locomotor recovery from MPTP insult after exposure to radiofrequency electromagnetic fields. Sci. Rep. 9:1201. doi:10.1038/s41598-018-37874-z.
   PubMed Web of Science ®Google Scholar
• Kim, J. H., U. D. Sohn, H. G. Kim, and H. R. Kim. 2018. Exposure to 835 MHz RF-EMF decreases the expression of calcium channels, inhibits apoptosis, but induces autophagy in the mouse hippocampus. Korean J. Physiol. Pharmacol. 22:277–89. doi:10.4196/kjpp.2018.22.3.277.
   PubMed Web of Science ®Google Scholar
• Kim, J. H., D. H. Yu, Y. H. Huh, E. H. Lee, H. G. Kim, and H. R. Kim. 2017. Long-term exposure to 835 MHz RF-EMF induces hyperactivity, autophagy and demyelination in the cortical neurons of mice. Sci. Rep. 7:41129. doi:10.1038/srep41129.
   PubMed Web of Science ®Google Scholar
• Lee, K. Y., B. C. Kim, N. K. Han, Y. S. Lee, T. Kim, J. H. Yun, N. Kim, J. K. Pack, and J. S. Lee. 2011. Effects of combined radiofrequency radiation exposure on the cell cycle and its regulatory proteins. Bioelectromagnetics 32:169–78. doi:10.1002/bem.20618.
   PubMed Web of Science ®Google Scholar
• Liu, Y.-X., J.-L. Tai, G.-Q. Li, Z.-W. Zhang, J.-H. Xue, H.-S. Liu, H. Zhu, Y.-L. Liu, A.-M. Li, and Y. Zhang. 2012. Exposure to 1950-MHz TD-SCDMA electromagnetic fields affects the apoptosis of astrocytes via caspase-3-dependent pathway. PloS One 7:e42332. doi:10.1371/journal.pone.0042332.
   PubMed Web of Science ®Google Scholar
• Malumbres, M. 2014. Cyclin-dependent kinases. Genome Biol. 15:122. doi:10.1186/gb4184.
   PubMed Web of Science ®Google Scholar
• Marchesi, N., C. Osera, L. Fassina, M. Amadio, F. Angeletti, M. Morini, G. Magenes, L. Venturini, M. Biggiogera, and G. Ricevuti. 2014. Autophagy is modulated in human neuroblastoma cells through direct exposition to low frequency electromagnetic fields. J. Cell. Physiol. 229:1776–86. doi:10.1002/jcp.24631.
   PubMed Web of Science ®Google Scholar
• Maskey, D., J. Pradhan, B. Aryal, C.-M. Lee, I.-Y. Choi, K.-S. Park, S. B. Kim, H. G. Kim, and M. J. Kim. 2010. Chronic 835-MHz radiofrequency exposure to mice hippocampus alters the distribution of calbindin and GFAP immunoreactivity. Brain Res. 1346:237–46. doi:10.1016/j.brainres.2010.05.045.
   PubMed Web of Science ®Google Scholar
• Miller, A. B., L. L. Morgan, I. Udasin, and D. L. Davis. 2018. Cancer epidemiology update, following the 2011 IARC evaluation of radiofrequency electromagnetic fields (Monograph 102). Environ. Res. 167:673–83. doi:10.1016/j.envres.2018.06.043.
   PubMed Web of Science ®Google Scholar
• NTP, Natioanl Toxicology Program.. 2018a. Toxicology and carcinogenesis studies in B6C3F1/N mice exposed to whole-body radio frequency radiation at a frequency (1,900 MHz) and modulations (GSM and CDMA) used by cell phones. Natl. Toxicol. Program Tech. Rep. Ser. 596(NTP–TR–596):1–270.
   Google Scholar
• NTP, National Toxicology Program. 2018b. NTP technical report on the toxicology and carcinogenesis studies in Hsd: Sprague Dawley sd rats exposed to whole-body radio frequency radiation at a frequency (900 MHz) and modulations (GSM and CDMA) used by cell phones. Natl. Toxicol. Program Tech. Rep. (Peer Review Draft) 595(NTP–TR–595):1–381.
   Google Scholar
• Nunes, H. L., K. Tuttis, J. M. Serpeloni, J. R. Nascimento, C. Q. Rocha, V. Al., O. Silva, A. H. Lengert, R. M. Reis, and I. M. S. Cólus. 2020. Characterization of the in vitro cytotoxic effects of brachydins isolated from Fridericia platyphylla in a prostate cancer cell line. J. Toxicol. Environ. Health A 83:547–58. doi:10.1080/15287394.2020.1784339.
   PubMedGoogle Scholar
• Ozelin, S. D., J. M. Senedese, J. M. Alves, C. C. Munari, J. C. Costa, F. A. Resende, D. L. Campos, I. M. S. Lima, A. F. Andrade, E. A. Varanda, et al.. 2021. Preventive activity of Copaifera langsdorffii Desf. leaves extract and its major compounds, afzelin and quercitrin, on DNA damage in in vitro and in vivo models. J. Toxicol. Environ. Health A 84:569–81. doi:10.1080/15287394.2021.1898505.
   PubMed Web of Science ®Google Scholar
• Paternot, S., T. Arsenijevic, K. Coulonval, L. Bockstaele, J. E. Dumont, and P. P. Roger. 2006. Distinct specificities of pRb phosphorylation by CDK4 activated by cyclin D1 or cyclin D3: Differential involvement in the distinct mitogenic modes of thyroid epithelial cells. Cell Cycle 5:61–70. doi:10.4161/cc.5.1.2265.
   PubMed Web of Science ®Google Scholar
• Quadros, A. P. O., L. M. Almeida, M. Petreanu, R. Niero, P. C. Pi. Rosa, A. C. H. F. Sawaya, M. S. Mantovani, I. O. M. Gaivão, and E. L. Maistro. 2020. Risk assessment via genotoxicity, metabolism, apoptosis, and cell growth effects in a HepG2/C3A cell line upon treatment with Rubus rosifolius (Rosaceae) leaves extract. J. Toxicol. Environ. Health A 83::495–508. doi:10.1080/15287394.2020.1779888.
   PubMed Web of Science ®Google Scholar
• Rafalski, V. A., and A. Brunet. 2011. Energy metabolism in adult neural stem cell fate. Prog. Neurobiol. 93:182–203.
   PubMed Web of Science ®Google Scholar
• Redmayne, M., and O. Johansson. 2014. Could myelin damage from radiofrequency electromagnetic field exposure help explain the functional impairment electrohypersensitivity? A review of the evidence. J. Toxicol. Environ. Health B 17:247–58. doi:10.1080/10937404.2014.923356.
   PubMed Web of Science ®Google Scholar
• Sagar, S., S. Dongus, A. Schoeni, K. Roser, M. Eeftens, B. Struchen, M. Foerster, N. Meier, S. Adem, and M. Röösli. 2018. Radiofrequency electromagnetic field exposure in everyday microenvironments in Europe: A systematic literature review. J. Expo. Sci. Environ. Epidemiol. 28:147–60. doi:10.1038/jes.2017.13.
   PubMed Web of Science ®Google Scholar
• Santini, S. J., V. Cordone, S. Falone, M. Mijit, C. Tatone, F. Amicarelli, and G. Di Emidio. 2018. Role of mitochondria in the oxidative stress induced by electromagnetic fields: Focus on reproductive systems. Oxid. Med. Cell. Longev. 2018:5076271. doi:10.1155/2018/5076271.
   PubMed Web of Science ®Google Scholar
• Selbach, M. T., A. S. Scotti, C. C. Feistel, C. C. Nicolau, D. Dalberto, N. G. dos Santos, G. Borsoi, A. B. F. Ferraz, I. Grivicich, G. M. S. de Souza, et al.. 2021. Evaluation of the cytotoxic and genotoxic effects of Sida planicaulis Cav extract using human neuroblastoma cell line SH-SY5Y. J. Toxicol. Environ. Health A 84:345–55. doi:10.1080/15287394.2020.1871144.
   PubMed Web of Science ®Google Scholar
• Soffritti, M., and L. Giuliani. 2019. The carcinogenic potential of non-ionizing radiations: The cases of S-50 Hz MF and 1.8 GHz GSM radiofrequency radiation. Basic Clin. Pharmacol. Toxicol. 125 (Suppl 3):58–69. doi:10.1111/bcpt.13215.
   PubMedGoogle Scholar
• Speidel, D. 2015. The role of DNA damage responses in p53 biology. Arch. Toxicol. 89:501–17.
   PubMed Web of Science ®Google Scholar
• Su, L., X. Wei, Z. Xu, and G. Chen. 2017. RF‐EMF exposure at 1800 MHz did not elicit DNA damage or abnormal cellular behaviors in different neurogenic cells. Bioelectromagnetics 38:175–85. doi:10.1002/bem.22032.
   PubMed Web of Science ®Google Scholar
• von Niederhäusern, N., A. Ducray, J. Zielinski, M. Murbach, and M. Mevissen. 2019. Effects of radiofrequency electromagnetic field exposure on neuronal differentiation and mitochondrial function in SH-SY5Y cells. Toxicol. In Vitro 61:104609. doi:10.1016/j.tiv.2019.104609.
   PubMed Web of Science ®Google Scholar
• Wade Harper, J., G. R. Adami, N. Wei, K. Keyomarsi, and S. J. Elledge. 1993. The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell 75:805–16. doi:10.1016/0092-8674(93)90499-G.
   PubMed Web of Science ®Google Scholar
• Wall, S., Z.-M. Wang, T. Kendig, D. Dobraca, and M. Lipsett. 2019. Real-world cell phone radiofrequency electromagnetic field exposures. Environ. Res. 171:581–92. doi:10.1016/j.envres.2018.09.015.
   PubMed Web of Science ®Google Scholar
• Xu, F., L. Na, Y. Li, and L. Chen. 2020. Roles of the PI3K/AKT/mTOR signalling pathways in neurodegenerative diseases and tumours. Cell Biosci. 10:1–12. doi:10.1186/s13578-020-00416-0.
   PubMed Web of Science ®Google Scholar
• Xu, S., G. Chen, C. Chen, C. Sun, D. Zhang, M. Murbach, N. Kuster, Q. Zeng, and Z. Xu. 2013. Cell type-dependent induction of DNA damage by 1800 MHz radiofrequency electromagnetic fields does not result in significant cellular dysfunctions. PLoS One 8:e54906. doi:10.1371/journal.pone.0054906.
   PubMed Web of Science ®Google Scholar
• Xu, S., Z. Zhou, L. Zhang, Z. Yu, W. Zhang, Y. Wang, X. Wang, M. Li, Y. Chen, and C. Chen. 2010. Exposure to 1800 MHz radiofrequency radiation induces oxidative damage to mitochondrial DNA in primary cultured neurons. Brain Res. 1311:189–96. doi:10.1016/j.brainres.2009.10.062.
   PubMed Web of Science ®Google Scholar
• Yogosawa, S., and K. Yoshida. 2018. Tumor suppressive role for kinases phosphorylating p53 in DNA damage‐induced apoptosis. Cancer Sci. 109:3376–82. doi:10.1111/cas.13792.
   PubMed Web of Science ®Google Scholar
• Zarkowska, T., and S. Mittnacht. 1997. Differential phosphorylation of the retinoblastoma protein by G1/S cyclin-dependent kinases. J. Biol. Chem. 272:12738–46. doi:10.1074/jbc.272.19.12738.
   PubMed Web of Science ®Google Scholar