Can 900 MHz and 2100 MHz radiofrequency radiation exposure induce endoplasmic reticulum stress and apoptosis in rat thymus?

Ergi Kaya; Esma Kırımlıoğlu; Hakan Er; Aslı Okan; Şükrü Özen; Necdet Demir

doi:10.18621/eurj.1049381

Research Article

Can 900 MHz and 2100 MHz radiofrequency radiation exposure induce endoplasmic reticulum stress and apoptosis in rat thymus?

Year 2023, Volume: 9 Issue: 1, 29 - 38, 04.01.2023

Ergi Kaya Esma Kırımlıoğlu Hakan Er Aslı Okan Şükrü Özen Necdet Demir

https://doi.org/10.18621/eurj.1049381

Abstract

Objectives: Electrical appliances are source of radiofrequency radiation (RFR). The effects of RFR on the organism are not fully understood. Endoplasmic reticulum (ER) stress is appeared by the accumulation of misfolded proteins in ER lumen. The aim of this study was to investigate the effects of 900 and 2100 MHz RFR exposure on the ER stress pathway in rat thymus.

Methods: Rats were divided into six groups: 1 week (w) and 10 w Sham rats were kept in plexiglass tubes for 2 hours/day without RFR, experiment groups were created as 1-w (acute) and 10 w (chronic) rats which exposed to 900 and 2100 MHz RFR for 2 h/day. There were 20 male Wistar rats in each group. Immunohistochemistry stainings were performed GRP78, CHOP, Cleaved (Clv.) Caspase 3 and Caspase 12.

Results: Expressions of GRP78 and Clv. Caspase3 in RFR groups is significantly higher than sham groups (p < 0.001). In 900 MHZ-1 w rats, high levels of GRP78 expressions were at the cytoplasm of epithelial reticular cells. In other groups, GRP78 expressions were seen also at thymocytes. Expressions of CHOP in RFR rats were higher than sham rats (2100 MHz /Sham for 10 w; p < 0.001, 900 MHz /Sham for 10 w; p = 0.004, 900 MHz /Sham for 1 w; p = 0.003). Localization of CHOP expressions was at the nucleus membrane and cytoplasm. The expression of Caspase 12 in RFR rats was higher than sham rats (900 MHz /Sham for 1 w; p = 0.006, other groups; p < 0.001).

Conclusions: This study demonstrates RFR exposure could increase levels of ER stress pathway proteins and could cause apoptosis.

Keywords

Radiofrequency radiation, thymus, endoplasmic reticulum stress, apoptosis

Supporting Institution

TUBITAK (SCIENTIFIC AND TECHNOLOGICAL RESEARCH INSTITUTION OF TURKEY) 2209-A University Students Research Project

Project Number

1919B011603479

References

1. Almanza A, Carlesso A, Chintha C, Creedican S, Doultsinos D, Leuzzi B, et al. Endoplasmic reticulum stress signalling - from basic mechanisms to clinical applications. FEBS J 2019;286:241-78.
2. Karagöz GA, Acosta-Alvear D, Walter P. The unfolded protein response: detecting and responding to fluctuations in the protein-folding capacity of the endoplasmic reticulum. Cold Spring Harb Perspect Biol 2019;11:a033886.
3. Zhu G, Lee AS. Role of the unfolded protein response, GRP78 and GRP94 in organ homeostasis. J Cell Physiol 2015;230:1413-20.
4. McQuiston A, Diehl JA. Recent insights into PERK-dependent signaling from the stressed endoplasmic reticulum. F1000Res 2017;6:1897.
5. Adams CJ, Kopp MC, Larburu N, Nowak PR, Ali MMU. Structure and molecular mechanism of ER stress signaling by the unfolded protein response signal activator IRE1. Front Mol Biosci 2019;6:11.
6. Hillary RF, FitzGerald U. A lifetime of stress: ATF6 in development and homeostasis. J Biomed Sci 2018;25:48.
7. Ahlbom A, Bridges J, de Seze R, Hillert L, Juutilainen J, Mattsson MO, et al. Possible effects of electromagnetic fields (EMF) on human health--opinion of the scientific committee on emerging and newly identified health risks (SCENIHR). Toxicology 2008;246:248-50.
8. Aydin B, Akar A. Effects of a 900-MHz electromagnetic field on oxidative stress parameters in rat lymphoid organs, polymorphonuclear leukocytes and plasma. Arch Med Res 2011;42:261-7.
9. Hancı H, Türedi S, Topal Z, Mercantepe T, Bozkurt I, Kaya H, et al. Can prenatal exposure to a 900 MHz electromagnetic field affect the morphology of the spleen and thymus, and alter biomarkers of oxidative damage in 21-day-old male rats? Biotech Histochem 2015;90:535-43.
10. Kulaber A, Kerimoğlu G, Ersöz Ş, Çolakoğlu S, Odacı E. Alterations of thymic morphology and antioxidant biomarkers in 60-day-old male rats following exposure to a continuous 900 MHz electromagnetic field during adolescence. Biotech Histochem 2017;92:331-7.
11. Kerimoğlu G, Güney C, Ersöz Ş, Odacı E. A histopathological and biochemical evaluation of oxidative injury in the sciatic nerves of male rats exposed to a continuous 900-megahertz electromagnetic field throughout all periods of adolescence. J Chem Neuroanat 2018;91:1-7.
12. Misa-Agustiño MJ, Leiro-Vidal JM, Gomez-Amoza JL, Jorge-Mora MT, Jorge-Barreiro FJ, Salas-Sánchez AA, et al. EMF radiation at 2450 MHz triggers changes in the morphology and expression of heat shock proteins and glucocorticoid receptors in rat thymus. Life Sci 2015;127:1-11.
13. Burkhardt M, Spinelli Y, Kuster N. Exposure setup to test effects of wireless communications systems on the CNS. Health Phys 1997;73:770-8.
14. Fritze K, Wiessner C, Kuster N, Sommer C, Gass P, Hermann DM, et al. Effect of global system for mobile communication microwave exposure on the genomic response of the rat brain. Neuroscience 1997;81:627-39.
15. Schönborn F, Poković K, Kuster N. Dosimetric analysis of the carousel setup for the exposure of rats at 1.62 GHz. Bioelectromagnetics 2004;25:16-26.
16. Weiland T. [A discretization model for the solution of Maxwell's equations for six-component fields]. Int J Electron Commun 1977;31:116-20. [Article in German]
17. Razi-Kazemi AA, Haijan M. Probabilistic assessment of ground potential rise using finite integration technique. IEEE Trans Power Delivery 2018;33:2452-61.
18. Gabriel S, Lau RW, Gabriel C. The dielectric properties of biological tissues: II. measurements in the frequency range 10 Hz to 20 GHz. Phys Med Biol 1996;41:2251-69.
19. Abdilla L, Sammut C, Mangion LZ. Dielectric properties of muscle and liver from 500 MHz-40 GHz. Electromagn Biol Med 2013;32:244-52.
20. Liu YX, Tai JL, Li GQ, Zhang ZW, Xue JH, Liu HS, et al. Exposure to 1950-MHz TD-SCDMA electromagnetic fields affects the apoptosis of astrocytes via caspase-3-dependent pathway. PLoS One 2012;7:e42332.
21. Joubert V, Leveque P, Cueille M, Bourthoumieu S, Yardin C. No apoptosis is induced in rat cortical neurons exposed to GSM phone fields. Bioelectromagnetics 2007;28:115-21.
22. Saygin M, Caliskan S, Karahan N, Koyu A, Gumral N, Uguz A. Testicular apoptosis and histopathological changes induced by a 2.45 GHz electromagnetic field. Toxicol Ind Health 2011;27:455-63.
23. Shokri S, Soltani A, Kazemi M, Sardari D, Mofrad FB. Effects of Wi-Fi (2.45 GHz) exposure on apoptosis, sperm parameters and testicular histomorphometry in rats: a time course study. Cell J 2015;17:322-31.
24. Odacı E, Hancı H, Yuluğ E, Türedi S, Aliyazıcıoğlu Y, Kaya H, et al. Effects of prenatal exposure to a 900 MHz electromagnetic field on 60-day-old rat testis and epididymal sperm quality. Biotech Histochem 2016;91:9-19.
25. Sehitoglu I, Tumkaya L, Kalkan Y, Bedir R, Cure MC, Zorba OU, et al. Biochemical and histopathological effects on the rat testis after exposure to electromagnetic field during fetal period. Arch Esp Urol 2015;68:562-8.
26. Odacı E, Özyılmaz C. Exposure to a 900 MHz electromagnetic field for 1 hour a day over 30 days does change the histopathology and biochemistry of the rat testis. Int J Radiat Biol 2015;91:547-54.
27. Hancı H, Odacı E, Kaya H, Aliyazıcıoğlu Y, Turan İ, Demir S, et al. The effect of prenatal exposure to 900-MHz electromagnetic field on the 21-old-day rat testicle. Reprod Toxicol 2013;42:203-9.
28. Kumar S, Kesari KK, Behari J. The therapeutic effect of a pulsed electromagnetic field on the reproductive patterns of male Wistar rats exposed to a 2.45-GHz microwave field. Clinics (Sao Paulo) 2011;66:1237-45.
29. Bedir R, Tumkaya L, Mercantepe T, Yilmaz A. Pathological findings observed in the kidneys of postnatal male rats exposed to the 2100 MHz electromagnetic field. Arch Med Res 2018;49:432-40.
30. Kuybulu AE, Öktem F, Çiriş İM, Sutcu R, Örmeci AR, Çömlekçi S, et al. Effects of long-term pre- and post-natal exposure to 2.45 GHz wireless devices on developing male rat kidney. Ren Fail 2016;38:571-80.
31. Bedir R, Tumkaya L, Şehitoğlu İ, Kalkan Y, Yilmaz A, Şahin OZ. The effect of exposure of rats during prenatal period to radiation spreading from mobile phones on renal development. Ren Fail 2015;37:305-9.
32. Odacı E, Ünal D, Mercantepe T, Topal Z, Hancı H, Türedi S, et al. Pathological effects of prenatal exposure to a 900 MHz electromagnetic field on the 21-day-old male rat kidney. Biotech Histochem 2015;90:93-101.
33. Okatan DÖ, Okatan AE, Hancı H, Demir S, Yaman SÖ, Çolakoğlu S, et al. Effects of 900-MHz electromagnetic fields exposure throughout middle/late adolescence on the kidney morphology and biochemistry of the female rat. Toxicol Ind Health 2018;34:693-702.
34. Okatan DÖ, Kaya H, Aliyazıcıoğlu Y, Demir S, Çolakoğlu S, Odacı E. Continuous 900-megahertz electromagnetic field applied in middle and late-adolescence causes qualitative and quantitative changes in the ovarian morphology, tissue and blood biochemistry of the rat. Int J Radiat Biol 2018;94:186-98.
35. Türedi S, Hancı H, Topal Z, Ünal D, Mercantepe T, Bozkurt İ, et al. The effects of prenatal exposure to a 900-MHz electromagnetic field on the 21-day-old male rat heart. Electromagn Biol Med 2015;34:390-7.
36. Kerimoğlu G, Mercantepe T, Erol HS, Turgut A, Kaya H, Çolakoğlu S, et al. Effects of long-term exposure to 900 megahertz electromagnetic field on heart morphology and biochemistry of male adolescent rats. Biotech Histochem 2016;91:445-54.
37. Gumral N, Saygin M, Asci H, Uguz AC, Celik O, Doguc DK, et al. The effects of electromagnetic radiation (2450 MHz wireless devices) on the heart and blood tissue: role of melatonin. Bratisl Lek Listy 2016;117:665-71.
38. Ragy MM. Effect of exposure and withdrawal of 900-MHz-electromagnetic waves on brain, kidney and liver oxidative stress and some biochemical parameters in male rats. Electromagn Biol Med 2015;34:279-84.
39. Topal Z, Hanci H, Mercantepe T, Erol HS, Keleş ON, Kaya H, et al. The effects of prenatal long-duration exposure to 900-MHz electromagnetic field on the 21-day-old newborn male rat liver. Turk J Med Sci 2015;45:291-7.
40. Okatan DÖ, Kulaber A, Kerimoglu G, Odacı E. Altered morphology and biochemistry of the female rat liver following 900 megahertz electromagnetic field exposure during mid to late adolescence. Biotech Histochem 2019;94:420-8.
41. Ohtani S, Ushiyama A, Maeda M, Ogasawara Y, Wang J, Kunugita N, et al. The effects of radio-frequency electromagnetic fields on T cell function during development. J Radiat Res 2015;56:467-74.

Year 2023, Volume: 9 Issue: 1, 29 - 38, 04.01.2023

Ergi Kaya Esma Kırımlıoğlu Hakan Er Aslı Okan Şükrü Özen Necdet Demir

https://doi.org/10.18621/eurj.1049381

Abstract

Project Number

1919B011603479

References

1. Almanza A, Carlesso A, Chintha C, Creedican S, Doultsinos D, Leuzzi B, et al. Endoplasmic reticulum stress signalling - from basic mechanisms to clinical applications. FEBS J 2019;286:241-78.
2. Karagöz GA, Acosta-Alvear D, Walter P. The unfolded protein response: detecting and responding to fluctuations in the protein-folding capacity of the endoplasmic reticulum. Cold Spring Harb Perspect Biol 2019;11:a033886.
3. Zhu G, Lee AS. Role of the unfolded protein response, GRP78 and GRP94 in organ homeostasis. J Cell Physiol 2015;230:1413-20.
4. McQuiston A, Diehl JA. Recent insights into PERK-dependent signaling from the stressed endoplasmic reticulum. F1000Res 2017;6:1897.
5. Adams CJ, Kopp MC, Larburu N, Nowak PR, Ali MMU. Structure and molecular mechanism of ER stress signaling by the unfolded protein response signal activator IRE1. Front Mol Biosci 2019;6:11.
6. Hillary RF, FitzGerald U. A lifetime of stress: ATF6 in development and homeostasis. J Biomed Sci 2018;25:48.
7. Ahlbom A, Bridges J, de Seze R, Hillert L, Juutilainen J, Mattsson MO, et al. Possible effects of electromagnetic fields (EMF) on human health--opinion of the scientific committee on emerging and newly identified health risks (SCENIHR). Toxicology 2008;246:248-50.
8. Aydin B, Akar A. Effects of a 900-MHz electromagnetic field on oxidative stress parameters in rat lymphoid organs, polymorphonuclear leukocytes and plasma. Arch Med Res 2011;42:261-7.
9. Hancı H, Türedi S, Topal Z, Mercantepe T, Bozkurt I, Kaya H, et al. Can prenatal exposure to a 900 MHz electromagnetic field affect the morphology of the spleen and thymus, and alter biomarkers of oxidative damage in 21-day-old male rats? Biotech Histochem 2015;90:535-43.
10. Kulaber A, Kerimoğlu G, Ersöz Ş, Çolakoğlu S, Odacı E. Alterations of thymic morphology and antioxidant biomarkers in 60-day-old male rats following exposure to a continuous 900 MHz electromagnetic field during adolescence. Biotech Histochem 2017;92:331-7.
11. Kerimoğlu G, Güney C, Ersöz Ş, Odacı E. A histopathological and biochemical evaluation of oxidative injury in the sciatic nerves of male rats exposed to a continuous 900-megahertz electromagnetic field throughout all periods of adolescence. J Chem Neuroanat 2018;91:1-7.
12. Misa-Agustiño MJ, Leiro-Vidal JM, Gomez-Amoza JL, Jorge-Mora MT, Jorge-Barreiro FJ, Salas-Sánchez AA, et al. EMF radiation at 2450 MHz triggers changes in the morphology and expression of heat shock proteins and glucocorticoid receptors in rat thymus. Life Sci 2015;127:1-11.
13. Burkhardt M, Spinelli Y, Kuster N. Exposure setup to test effects of wireless communications systems on the CNS. Health Phys 1997;73:770-8.
14. Fritze K, Wiessner C, Kuster N, Sommer C, Gass P, Hermann DM, et al. Effect of global system for mobile communication microwave exposure on the genomic response of the rat brain. Neuroscience 1997;81:627-39.
15. Schönborn F, Poković K, Kuster N. Dosimetric analysis of the carousel setup for the exposure of rats at 1.62 GHz. Bioelectromagnetics 2004;25:16-26.
16. Weiland T. [A discretization model for the solution of Maxwell's equations for six-component fields]. Int J Electron Commun 1977;31:116-20. [Article in German]
17. Razi-Kazemi AA, Haijan M. Probabilistic assessment of ground potential rise using finite integration technique. IEEE Trans Power Delivery 2018;33:2452-61.
18. Gabriel S, Lau RW, Gabriel C. The dielectric properties of biological tissues: II. measurements in the frequency range 10 Hz to 20 GHz. Phys Med Biol 1996;41:2251-69.
19. Abdilla L, Sammut C, Mangion LZ. Dielectric properties of muscle and liver from 500 MHz-40 GHz. Electromagn Biol Med 2013;32:244-52.
20. Liu YX, Tai JL, Li GQ, Zhang ZW, Xue JH, Liu HS, et al. Exposure to 1950-MHz TD-SCDMA electromagnetic fields affects the apoptosis of astrocytes via caspase-3-dependent pathway. PLoS One 2012;7:e42332.
21. Joubert V, Leveque P, Cueille M, Bourthoumieu S, Yardin C. No apoptosis is induced in rat cortical neurons exposed to GSM phone fields. Bioelectromagnetics 2007;28:115-21.
22. Saygin M, Caliskan S, Karahan N, Koyu A, Gumral N, Uguz A. Testicular apoptosis and histopathological changes induced by a 2.45 GHz electromagnetic field. Toxicol Ind Health 2011;27:455-63.
23. Shokri S, Soltani A, Kazemi M, Sardari D, Mofrad FB. Effects of Wi-Fi (2.45 GHz) exposure on apoptosis, sperm parameters and testicular histomorphometry in rats: a time course study. Cell J 2015;17:322-31.
24. Odacı E, Hancı H, Yuluğ E, Türedi S, Aliyazıcıoğlu Y, Kaya H, et al. Effects of prenatal exposure to a 900 MHz electromagnetic field on 60-day-old rat testis and epididymal sperm quality. Biotech Histochem 2016;91:9-19.
25. Sehitoglu I, Tumkaya L, Kalkan Y, Bedir R, Cure MC, Zorba OU, et al. Biochemical and histopathological effects on the rat testis after exposure to electromagnetic field during fetal period. Arch Esp Urol 2015;68:562-8.
26. Odacı E, Özyılmaz C. Exposure to a 900 MHz electromagnetic field for 1 hour a day over 30 days does change the histopathology and biochemistry of the rat testis. Int J Radiat Biol 2015;91:547-54.
27. Hancı H, Odacı E, Kaya H, Aliyazıcıoğlu Y, Turan İ, Demir S, et al. The effect of prenatal exposure to 900-MHz electromagnetic field on the 21-old-day rat testicle. Reprod Toxicol 2013;42:203-9.
28. Kumar S, Kesari KK, Behari J. The therapeutic effect of a pulsed electromagnetic field on the reproductive patterns of male Wistar rats exposed to a 2.45-GHz microwave field. Clinics (Sao Paulo) 2011;66:1237-45.
29. Bedir R, Tumkaya L, Mercantepe T, Yilmaz A. Pathological findings observed in the kidneys of postnatal male rats exposed to the 2100 MHz electromagnetic field. Arch Med Res 2018;49:432-40.
30. Kuybulu AE, Öktem F, Çiriş İM, Sutcu R, Örmeci AR, Çömlekçi S, et al. Effects of long-term pre- and post-natal exposure to 2.45 GHz wireless devices on developing male rat kidney. Ren Fail 2016;38:571-80.
31. Bedir R, Tumkaya L, Şehitoğlu İ, Kalkan Y, Yilmaz A, Şahin OZ. The effect of exposure of rats during prenatal period to radiation spreading from mobile phones on renal development. Ren Fail 2015;37:305-9.
32. Odacı E, Ünal D, Mercantepe T, Topal Z, Hancı H, Türedi S, et al. Pathological effects of prenatal exposure to a 900 MHz electromagnetic field on the 21-day-old male rat kidney. Biotech Histochem 2015;90:93-101.
33. Okatan DÖ, Okatan AE, Hancı H, Demir S, Yaman SÖ, Çolakoğlu S, et al. Effects of 900-MHz electromagnetic fields exposure throughout middle/late adolescence on the kidney morphology and biochemistry of the female rat. Toxicol Ind Health 2018;34:693-702.
34. Okatan DÖ, Kaya H, Aliyazıcıoğlu Y, Demir S, Çolakoğlu S, Odacı E. Continuous 900-megahertz electromagnetic field applied in middle and late-adolescence causes qualitative and quantitative changes in the ovarian morphology, tissue and blood biochemistry of the rat. Int J Radiat Biol 2018;94:186-98.
35. Türedi S, Hancı H, Topal Z, Ünal D, Mercantepe T, Bozkurt İ, et al. The effects of prenatal exposure to a 900-MHz electromagnetic field on the 21-day-old male rat heart. Electromagn Biol Med 2015;34:390-7.
36. Kerimoğlu G, Mercantepe T, Erol HS, Turgut A, Kaya H, Çolakoğlu S, et al. Effects of long-term exposure to 900 megahertz electromagnetic field on heart morphology and biochemistry of male adolescent rats. Biotech Histochem 2016;91:445-54.
37. Gumral N, Saygin M, Asci H, Uguz AC, Celik O, Doguc DK, et al. The effects of electromagnetic radiation (2450 MHz wireless devices) on the heart and blood tissue: role of melatonin. Bratisl Lek Listy 2016;117:665-71.
38. Ragy MM. Effect of exposure and withdrawal of 900-MHz-electromagnetic waves on brain, kidney and liver oxidative stress and some biochemical parameters in male rats. Electromagn Biol Med 2015;34:279-84.
39. Topal Z, Hanci H, Mercantepe T, Erol HS, Keleş ON, Kaya H, et al. The effects of prenatal long-duration exposure to 900-MHz electromagnetic field on the 21-day-old newborn male rat liver. Turk J Med Sci 2015;45:291-7.
40. Okatan DÖ, Kulaber A, Kerimoglu G, Odacı E. Altered morphology and biochemistry of the female rat liver following 900 megahertz electromagnetic field exposure during mid to late adolescence. Biotech Histochem 2019;94:420-8.
41. Ohtani S, Ushiyama A, Maeda M, Ogasawara Y, Wang J, Kunugita N, et al. The effects of radio-frequency electromagnetic fields on T cell function during development. J Radiat Res 2015;56:467-74.

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Details

Primary Language	English
Subjects	Biochemistry and Cell Biology (Other)
Journal Section	Original Articles
Authors	Ergi Kaya 0000-0001-9003-7066 Esma Kırımlıoğlu 0000-0002-5689-5670 Hakan Er 0000-0001-7739-4712 Aslı Okan 0000-0001-8152-7338 Şükrü Özen 0000-0002-5538-6786 Necdet Demir 0000-0002-8166-5535
Project Number	1919B011603479
Publication Date	January 4, 2023
Submission Date	August 23, 2022
Acceptance Date	October 17, 2022
Published in Issue	Year 2023 Volume: 9 Issue: 1

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AMA	Kaya E, Kırımlıoğlu E, Er H, Okan A, Özen Ş, Demir N. Can 900 MHz and 2100 MHz radiofrequency radiation exposure induce endoplasmic reticulum stress and apoptosis in rat thymus?. Eur Res J. January 2023;9(1):29-38. doi:10.18621/eurj.1049381

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