Abstract

Terahertz (THz) demethylation is a photomedical technique applied to dissociate methyl-DNA bonds and reduce global DNA methylation using resonant THz radiation. We evaluated the performance of THz demethylation and investigated the DNA damage caused by THz irradiation. The demethylation rate in M-293T DNA increased linearly with the irradiation power up to 48%. The degree of demethylation increased with exposure to THz radiation, saturating after 10 min. Although THz demethylation occurred globally, most of the demethylation occurred within the partial genes in the CpG islands. Subsequently, we performed THz demethylation of melanoma cells. The degree of methylation in the melanoma cell pellets decreased by approximately 10–15%, inducing ∼5–8 abasic sites per 105 bp; this was considerably less than the damaged DNA irradiated by the high-power infrared laser beam used for generating THz pulses. These results provide initial data for THz demethylation and demonstrate the applicability of this technique in advanced cancer cell research. THz demethylation has the potential to develop into a therapeutic procedure for cancer, similar to that involving chemical demethylating agents.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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References

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    [Crossref]
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2019 (5)

J.-H. Son, S. J. Oh, and H. Cheon, “Potential clinical applications of terahertz radiation,” J. Appl. Phys. 125(19), 190901 (2019).
[Crossref]

H. Cheon, J. H. Paik, M. Choi, H.-J. Yang, and J.-H. Son, “Detection and manipulation of methylation in blood cancer DNA using terahertz radiation,” Sci. Rep. 9(1), 6413 (2019).
[Crossref]

K. Nawata, Y. Tokizane, Y. Takida, and H. Minamide, “Tunable backward terahertz-wave parametric oscillation,” Sci. Rep. 9(1), 726 (2019).
[Crossref]

P. S. Nugraha, G. Krizsan, C. Lombosi, L. Palfalvi, G. Toth, G. Almasi, J. A. Fulop, and J. Hebling, “Demonstration of a tilted-pulse-front pumped plane-parallel slab terahertz source,” Opt. Lett. 44(4), 1023–1026 (2019).
[Crossref]

L. Bosco, M. Franckie, G. Scalari, M. Beck, A. Wacker, and J. Faist, “Thermoelectrically cooled THz quantum cascade laser operationg up to 210 K,” Appl. Phys. Lett. 115(1), 010601 (2019).
[Crossref]

2018 (1)

V. Franchini, S. De Sanctis, J. Marinaccio, A. De Amicis, E. Coluzzi, S. Di Cristofaro, F. Lista, E. Regalbuto, A. Doria, E. Giovenale, G. P. Gallerano, R. Bei, M. Benvenuto, L. Masuelli, I. Udroiu, and A. Sgura, “Study of the effects of 0.15 terahertz radiation on genome integrity of adult fibroblasts,” Environ. Mol. Mutagen. 59(6), 476–487 (2018).
[Crossref]

2017 (2)

H. Cheon, H.-J. Yang, and J.-H. Son, “Toward clinical cancer imaging using terahertz spectroscopy,” IEEE J. Sel. Top. Quantum Electron. 23(4), 1–9 (2017).
[Crossref]

J. F. Linnekamp, R. Butter, R. Spijker, J. P. Medema, and H. W. M. van Laarhoven, “Clinical and biological effects of demethylating agents on solid tumours – A systematic review,” Cancer Treat. Rev. 54, 10–23 (2017).
[Crossref]

2016 (3)

D. Roulois, H. L. Yau, and D. D. De Carvalho, “Pharmacological DNA demethylation: Implications for cancer immunotherapy,” OncoImmunology 5(3), e1090077 (2016).
[Crossref]

S. Kurdyukov and M. Bullock, “DNA methylation analysis: choosing the right method,” Biology (Basel, Switz.) 5(1), 3 (2016).
[Crossref]

H. Cheon, H. J. Yang, S. H. Lee, Y. A. Kim, and J.-H. Son, “Terahertz molecular resonance of cancer DNA,” Sci. Rep. 6(1), 37103 (2016).
[Crossref]

2015 (2)

D. J. Garama, T. J. Harris, C. L. White, F. J. Rossello, M. Abdul-Hay, D. J. Gough, and D. E. Levy, “A synthetic lethal interaction between glutathione synthesis and mitochondrial reactive oxygen species provides a tumor-specific vulnerability dependent on STAT3,” Mol. Cell. Biol. 35(21), 3646–3656 (2015).
[Crossref]

J. D. Licht, “DNA methylation inhibitors in cancer therapy: the immunity dimension,” Cell 162(5), 938–939 (2015).
[Crossref]

2014 (4)

J. S. Brodbelt, “Photodissociation mass spectrometry: New tools for characterization of biological molecules,” Chem. Soc. Rev. 43(8), 2757–2783 (2014).
[Crossref]

P. Malik and A. F. Cashen, “Decitabine in the treatment of acute myeloid leukemia in elderly patients,” Cancer Manage. Res. 6, 53–61 (2014).
[Crossref]

J. Andersen, J. Heimdal, D. W. Mahler, B. Nelander, and R. Wugt Larsen, “Communication: THz absorption spectrum of the CO2 -H2O complex: Observation and assignment of intermolecular van der Waals vibrations,” J. Chem. Phys. 140(9), 091103 (2014).
[Crossref]

S. J. Oh, S.-H. Kim, Y. Bin Ji, K. Jeong, Y. Park, J. Yang, D. W. Park, S. K. Noh, S.-G. Kang, Y.-M. Huh, J.-H. Son, and J.-S. Suh, “Study of freshly excised brain tissues using terahertz imaging,” Biomed. Opt. Express 5(8), 2837–2842 (2014).
[Crossref]

2013 (6)

C. B. Reid, G. Reese, A. P. Gibson, and V. P. Wallace, “Terahertz Time-Domain Spectroscopy of Human Blood,” IEEE J. Biomed. Health Inform. 17(4), 774–778 (2013).
[Crossref]

Y. G. Lee, I. Kim, S. S. Yoon, S. Park, J. W. Cheong, Y. H. Min, J. O. Lee, S. M. Bang, H. G. Yi, C. S. Kim, Y. Park, B. S. Kim, Y. C. Mun, C. M. Seong, J. Park, J. H. Lee, S. Y. Kim, H. G. Lee, Y. K. Kim, and H. J. Kim, “Comparative analysis between azacitidine and decitabine for the treatment of myelodysplastic syndromes,” Br. J. Haematol. 161(3), 339–347 (2013).
[Crossref]

L. V. Titova, A. K. Ayesheshim, A. Golubov, R. Rodriguez-Juarez, R. Woycicki, F. A. Hegmann, and O. Kovalchuk, “Intense THz pulses down-regulate genes associated with skin cancer and psoriasis: a new therapeutic avenue?” Sci. Rep. 3(1), 2363 (2013).
[Crossref]

E. Hervouet, M. Cheray, F. Vallette, and P.-F. Cartron, “DNA methylation and apoptosis resistance in cancer cells,” Cells 2(3), 545–573 (2013).
[Crossref]

S. J. Oh, S.-H. Kim, K. Jeong, Y. Park, Y.-M. Huh, J.-H. Son, and J.-S. Suh, “Measurement depth enhancement in terahertz imaging of biological tissues,” Opt. Express 21(18), 21299 (2013).
[Crossref]

Y. C. Sim, J. Y. Park, K.-M. Ahn, C. Park, and J.-H. Son, “Terahertz imaging of excised oral cancer at frozen temeprature,” Biomed. Opt. Express 4(8), 1413–1421 (2013).
[Crossref]

2012 (1)

K. W. Kim, H. Kim, J. Park, J. K. Han, and J. H. Son, “Terahertz tomographic imaging of transdermal drug delivery,” IEEE Trans. Terahertz Sci. Technol. 2(1), 99–106 (2012).
[Crossref]

2011 (3)

P. C. Taberlay and P. A. Jones, “DNA methylation and cancer,” Prog. Drug Res. 67, 1–23 (2011).

E. Zaika, J. Wei, D. Yin, C. Andl, U. Moll, W. El-Rifai, and A. I. Zaika, “p73 protein regulates DNA damage repair,” FASEB J. 25(12), 4406–4414 (2011).
[Crossref]

J. Ren, B. N. Singh, Q. Huang, Z. Li, Y. Gao, P. Mishra, Y. L. Hwa, J. Li, S. C. Dowdy, and S. W. Jiang, “DNA hypermethylation as a chemotherapy target,” Cell. Signalling 23(7), 1082–1093 (2011).
[Crossref]

2010 (2)

T. K. Kelly, D. D. De Carvalho, and P. A. Jones, “Epigenetic modifications as therapeutic targets,” Nat. Biotechnol. 28(10), 1069–1078 (2010).
[Crossref]

P. W. Hollenbach, A. N. Nguyen, H. Brady, M. Williams, Y. Ning, N. Richard, L. Krushel, S. L. Aukerman, C. Heise, and K. J. MacBeth, “A comparison of azacitidine and decitabine activities in acute myeloid leukemia cell lines,” PLoS One 5(2), e9001 (2010).
[Crossref]

2009 (1)

2008 (1)

A. Korenstein-Ilan, A. Barbul, P. Hasin, A. Eliran, A. Gover, and R. Korenstein, “Terahertz Radiation Increases Genomic Instability in Human Lymphocytes,” Radiat. Res. 170(2), 224–234 (2008).
[Crossref]

2006 (1)

M. W. Luczak and P. P. Jagodzinski, “The role of DNA methylation in cancer development,” Folia Histochem Cytobiol. 44(3), 143–154 (2006).

2005 (1)

A. Eramo, R. Pallini, F. Lotti, G. Sette, M. Patti, M. Bartucci, L. Ricci-Vitiani, M. Signore, G. Stassi, L. M. Larocca, L. Crinò, C. Peschle, and R. De Maria, “Inhibition of DNA methylation sensitizes glioblastoma for tumor necrosis factor-related apoptosis-inducing ligand-mediated destruction,” Cancer Res. 65(24), 11469–11477 (2005).
[Crossref]

2004 (2)

M. Szyf, P. Pakneshan, and S. A. Rabbani, “DNA methylation and breast cancer,” Biochem. Pharmacol. 68(6), 1187–1197 (2004).
[Crossref]

K. Wang and D. M. Mittleman, “Metal wires for terahertz wave guiding,” Nature 432(7015), 376–379 (2004).
[Crossref]

2003 (1)

M. Szyf, “DNA methylation and cancer therapy,” Drug Resist. Updat. 6, 341–353 (2003).
[Crossref]

2002 (3)

B. M. Fischer, M. Walther, and P. Uhd Jepsen, “Far-infrared vibrational modes of DNA components studied by terahertz time-domain spectroscopy,” Phys. Med. Biol. 47(21), 3807–3814 (2002).
[Crossref]

M. Walther, P. Plochocka, B. Fischer, H. Helm, and P. Uhd Jepsen, “Collective vibrational modes in biological molecules investigated by terahertz time-domain spectroscopy,” Biopolymers 67(4-5), 310–313 (2002).
[Crossref]

J. K. Christman, “5-Azacytidine and 5-aza-2’-deoxycytidine as inhibitors of DNA methylation: mechanistic studies and their implications for cancer therapy,” Oncogene 21(35), 5483–5495 (2002).
[Crossref]

1995 (1)

L. Thrane, R. H. Jacobsen, P. Uhd Jepsen, and S. R. Keiding, “THz reflection spectroscopy of liquid water,” Chem. Phys. Lett. 240(4), 330–333 (1995).
[Crossref]

1993 (1)

L. Tomas, “Instability and decay of the primary structure of DNA,” Nature 362(6422), 709–715 (1993).
[Crossref]

Abdul-Hay, M.

D. J. Garama, T. J. Harris, C. L. White, F. J. Rossello, M. Abdul-Hay, D. J. Gough, and D. E. Levy, “A synthetic lethal interaction between glutathione synthesis and mitochondrial reactive oxygen species provides a tumor-specific vulnerability dependent on STAT3,” Mol. Cell. Biol. 35(21), 3646–3656 (2015).
[Crossref]

Ahn, K.-M.

Almasi, G.

Andersen, J.

J. Andersen, J. Heimdal, D. W. Mahler, B. Nelander, and R. Wugt Larsen, “Communication: THz absorption spectrum of the CO2 -H2O complex: Observation and assignment of intermolecular van der Waals vibrations,” J. Chem. Phys. 140(9), 091103 (2014).
[Crossref]

Andl, C.

E. Zaika, J. Wei, D. Yin, C. Andl, U. Moll, W. El-Rifai, and A. I. Zaika, “p73 protein regulates DNA damage repair,” FASEB J. 25(12), 4406–4414 (2011).
[Crossref]

Aukerman, S. L.

P. W. Hollenbach, A. N. Nguyen, H. Brady, M. Williams, Y. Ning, N. Richard, L. Krushel, S. L. Aukerman, C. Heise, and K. J. MacBeth, “A comparison of azacitidine and decitabine activities in acute myeloid leukemia cell lines,” PLoS One 5(2), e9001 (2010).
[Crossref]

Ayesheshim, A. K.

L. V. Titova, A. K. Ayesheshim, A. Golubov, R. Rodriguez-Juarez, R. Woycicki, F. A. Hegmann, and O. Kovalchuk, “Intense THz pulses down-regulate genes associated with skin cancer and psoriasis: a new therapeutic avenue?” Sci. Rep. 3(1), 2363 (2013).
[Crossref]

Bang, S. M.

Y. G. Lee, I. Kim, S. S. Yoon, S. Park, J. W. Cheong, Y. H. Min, J. O. Lee, S. M. Bang, H. G. Yi, C. S. Kim, Y. Park, B. S. Kim, Y. C. Mun, C. M. Seong, J. Park, J. H. Lee, S. Y. Kim, H. G. Lee, Y. K. Kim, and H. J. Kim, “Comparative analysis between azacitidine and decitabine for the treatment of myelodysplastic syndromes,” Br. J. Haematol. 161(3), 339–347 (2013).
[Crossref]

Barbul, A.

A. Korenstein-Ilan, A. Barbul, P. Hasin, A. Eliran, A. Gover, and R. Korenstein, “Terahertz Radiation Increases Genomic Instability in Human Lymphocytes,” Radiat. Res. 170(2), 224–234 (2008).
[Crossref]

Bartucci, M.

A. Eramo, R. Pallini, F. Lotti, G. Sette, M. Patti, M. Bartucci, L. Ricci-Vitiani, M. Signore, G. Stassi, L. M. Larocca, L. Crinò, C. Peschle, and R. De Maria, “Inhibition of DNA methylation sensitizes glioblastoma for tumor necrosis factor-related apoptosis-inducing ligand-mediated destruction,” Cancer Res. 65(24), 11469–11477 (2005).
[Crossref]

Beck, M.

L. Bosco, M. Franckie, G. Scalari, M. Beck, A. Wacker, and J. Faist, “Thermoelectrically cooled THz quantum cascade laser operationg up to 210 K,” Appl. Phys. Lett. 115(1), 010601 (2019).
[Crossref]

Bei, R.

V. Franchini, S. De Sanctis, J. Marinaccio, A. De Amicis, E. Coluzzi, S. Di Cristofaro, F. Lista, E. Regalbuto, A. Doria, E. Giovenale, G. P. Gallerano, R. Bei, M. Benvenuto, L. Masuelli, I. Udroiu, and A. Sgura, “Study of the effects of 0.15 terahertz radiation on genome integrity of adult fibroblasts,” Environ. Mol. Mutagen. 59(6), 476–487 (2018).
[Crossref]

Benvenuto, M.

V. Franchini, S. De Sanctis, J. Marinaccio, A. De Amicis, E. Coluzzi, S. Di Cristofaro, F. Lista, E. Regalbuto, A. Doria, E. Giovenale, G. P. Gallerano, R. Bei, M. Benvenuto, L. Masuelli, I. Udroiu, and A. Sgura, “Study of the effects of 0.15 terahertz radiation on genome integrity of adult fibroblasts,” Environ. Mol. Mutagen. 59(6), 476–487 (2018).
[Crossref]

Bin Ji, Y.

Bosco, L.

L. Bosco, M. Franckie, G. Scalari, M. Beck, A. Wacker, and J. Faist, “Thermoelectrically cooled THz quantum cascade laser operationg up to 210 K,” Appl. Phys. Lett. 115(1), 010601 (2019).
[Crossref]

Brady, H.

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Figures (8)

Fig. 1.
Fig. 1. Schematic showing THz demethylation using resonant THz radiation system. High-power THz radiation was generated using a regenerative amplifier and LiNbO3 crystal. The THz filter limited the THz bandwidth to around the resonance frequency of the methyl-DNA bonds.
Fig. 2.
Fig. 2. Collection process of melanoma cell pellets. Absorption of THz radiation by water molecules was reduced in frozen cell pellets.
Fig. 3.
Fig. 3. Biological methods for verifying THz demethylation. (a) Bisulfite sequencing to quantify the degree of DNA methylation in partial genes. (b) Investigation of DNA damage by measuring AP sites, indicating the locations of missing nucleobases.
Fig. 4.
Fig. 4. Power dependency of THz demethylation in M-293 T DNA. (a) Degree of methylation decreased with increasing THz irradiation power. THz power was augmented via 10-µW increments, and we obtained each data point by averaging six OD values obtained via ELISA quantification. Error bars represent the standard deviation of each data point. (b) THz demethylation rate exhibiting linear dependency on the irradiation power (R2 = 0.97757).
Fig. 5.
Fig. 5. THz demethylation dependence on exposure time in M-293T DNA. Irradiation power was held constant at 40 µW. Below 15 min of exposure time, the degree of methylation decreased with longer exposure times; however, the rate began to saturate after 10 min, as observed in a previous study [6]. The measurements were repeated six times and averaged at each data point. Error bar indicates the standard deviation.
Fig. 6.
Fig. 6. Asymmetrical pattern of THz demethylation in partial genes. The demethylation ratio of genes at CpGI sites was much higher than that of the genes at non-CpG sites. Data were obtained through bisulfite sequencing of M-293 T DNA.
Fig. 7.
Fig. 7. THz demethylation of melanoma cell pellets (1–3). THz demethylation occurred within the natural cell structure. Data was averaged across four measurements. Error bars shows the standard deviation.
Fig. 8.
Fig. 8. DNA damage via THz demethylation in melanoma cell pellets. (a) Standard curve for measurement of AP sites. (b) Number of AP sites produced by THz demethylation. THz demethylation induced a few AP sites; however, there were fewer sites compared to the DNA damaged by infrared radiation. Error bars for each data point represent the standard deviation.