Abstract

Recent emergence and growing use of terahertz (THz) radiation for medical imaging and public security screening raise questions on reasonable levels of exposure and health consequences of this form of electromagnetic radiation. In particular, picosecond-duration THz pulses have shown promise for novel diagnostic imaging techniques. However, the effects of THz pulses on human cells and tissues thus far remain largely unknown. We report on the investigation of the biological effects of pulsed THz radiation on artificial human skin tissues. We observe that exposure to intense THz pulses for ten minutes leads to a significant induction of H2AX phosphorylation, indicating that THz pulse irradiation may cause DNA damage in exposed skin tissue. At the same time, we find a THz-pulse-induced increase in the levels of several proteins responsible for cell-cycle regulation and tumor suppression, suggesting that DNA damage repair mechanisms are quickly activated. Furthermore, we find that the cellular response to pulsed THz radiation is significantly different from that induced by exposure to UVA (400 nm).

© 2013 OSA

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2012 (3)

P. Reynolds, J. A. Anderson, J. V. Harper, M. A. Hill, S. W. Botchway, A. W. Parker, and P. O’Neill, “The dynamics of Ku70/80 and DNA-PKcs at DSBs induced by ionizing radiation is dependent on the complexity of damage,” Nucleic Acids Res.40(21), 10821–10831 (2012).
[CrossRef] [PubMed]

H. Chen, Y. Bao, L. Yu, R. Jia, W. Cheng, and C. Shao, “Comparison of cellular damage response to low-dose-rate 125I seed irradiation and high-dose-rate gamma irradiation in human lung cancer cells,” Brachytherapy11(2), 149–156 (2012).
[CrossRef] [PubMed]

T. Sperka, J. Wang, and K. L. Rudolph, “DNA damage checkpoints in stem cells, ageing and cancer,” Nat. Rev. Mol. Cell Biol.13(9), 579–590 (2012).
[CrossRef] [PubMed]

2011 (8)

Y. Zwang, A. Sas-Chen, Y. Drier, T. Shay, R. Avraham, M. Lauriola, E. Shema, E. Lidor-Nili, J. Jacob-Hirsch, N. Amariglio, Y. Lu, G. B. Mills, G. Rechavi, M. Oren, E. Domany, and Y. Yarden, “Two phases of mitogenic signaling unveil roles for p53 and EGR1 in elimination of inconsistent growth signals,” Mol. Cell42(4), 524–535 (2011).
[CrossRef] [PubMed]

B. S. Alexandrov, K. Ø. Rasmussen, A. R. Bishop, A. Usheva, L. B. Alexandrov, S. Chong, Y. Dagon, L. G. Booshehri, C. H. Mielke, M. L. Phipps, J. S. Martinez, H.-T. Chen, and G. Rodriguez, “Non-thermal effects of terahertz radiation on gene expression in mouse stem cells,” Biomed. Opt. Express2(9), 2679–2689 (2011).
[CrossRef] [PubMed]

P. U. Jepsen, D. G. Cooke, and M. Koch, “Terahertz spectroscopy and imaging — Modern techniques and applications,” Laser Photonics Rev.5(1), 124–166 (2011).
[CrossRef]

G. J. Wilmink and J. E. Grundt, “Current State of Research on Biological Effects of Terahertz Radiation,” J. Infrared Millim. Terahz Waves32(10), 1074–1122 (2011).
[CrossRef]

H. Hintzsche, C. Jastrow, T. Kleine-Ostmann, H. Stopper, E. Schmid, and T. Schrader, “Terahertz radiation induces spindle disturbances in human-hamster hybrid cells,” Radiat. Res.175(5), 569–574 (2011).
[CrossRef] [PubMed]

F. Blanchard, G. Sharma, L. Razzari, X. Ropagnol, H.-C. Bandulet, F. Vidal, R. Morandotti, J.-C. Kieffer, T. Ozaki, H. Tiedje, H. Haugen, M. Reid, and F. A. Hegmann, “Generation of intense terahertz radiation via optical methods,” IEEE J. Sel. Top. Quantum Electron.17(1), 5–16 (2011).
[CrossRef]

M. C. Hoffmann and J. A. Fülöp, “Intense ultrashort terahertz pulses: generation and applications,” J. Phys. D Appl. Phys.44(8), 083001 (2011).
[CrossRef]

J. S. Dickey, F. J. Zemp, A. Altamirano, O. A. Sedelnikova, W. M. Bonner, and O. Kovalchuk, “H2AX phosphorylation in response to DNA double-strand break formation during bystander signalling: effect of microRNA knockdown,” Radiat. Prot. Dosimetry143(2-4), 264–269 (2011).
[CrossRef] [PubMed]

2010 (9)

R. P. Rastogi, A. Richa, A. Kumar, M. B. Tyagi, and R. P. Sinha, “Molecular mechanisms of ultraviolet radiation-induced DNA damage and repair,” J. Nucleic Acids2010, 592980 (2010).
[CrossRef] [PubMed]

O. Kovalchuk, F. J. Zemp, J. N. Filkowski, A. M. Altamirano, J. S. Dickey, G. Jenkins-Baker, S. A. Marino, D. J. Brenner, W. M. Bonner, and O. A. Sedelnikova, “microRNAome changes in bystander three-dimensional human tissue models suggest priming of apoptotic pathways,” Carcinogenesis31(10), 1882–1888 (2010).
[CrossRef] [PubMed]

G. J. Wilmink, B. L. Ibey, C. L. Roth, R. L. Vincelette, B. D. Rivest, C. B. Horn, J. Bernhard, D. Roberson, and W. P. Roach, “Determination of death thresholds and identification of terahertz (THz) – specific gene expression signatures,” Proc. SPIE7562, 75620K, 75620K-8 (2010).
[CrossRef]

G. J. Wilmink, B. D. Rivest, B. L. Ibey, C. L. Roth, J. Bernhard, and W. P. Roach, “Quantitative investigation of bioeffects associated with terahertz radiation,” Proc. SPIE7562, 75620L, 75620L-10 (2010).
[CrossRef]

J. Bock, Y. Fukuyo, S. Kang, M. L. Phipps, L. B. Alexandrov, K. Ø. Rasmussen, A. R. Bishop, E. D. Rosen, J. S. Martinez, H.-T. Chen, G. Rodriguez, B. S. Alexandrov, and A. Usheva, “Mammalian stem cells reprogramming in response to terahertz radiation,” PLoS ONE5(12), e15806 (2010).
[CrossRef] [PubMed]

B. S. Alexandrov, V. Gelev, A. R. Bishop, A. Usheva, and K. O. Rasmussen, “DNA breathing dynamics in the presence of a terahertz field,” Phys. Lett. A374(10), 1214–1217 (2010).
[CrossRef] [PubMed]

M. Vasudev, J. Yang, H.-S. Jung, M. A. Stroscio, and M. Dutta, “Integrated nanostructure–semiconductor molecular complexes as tools for THz spectral studies of DNA,” IEEE Sens. J.10(3), 524–530 (2010).
[CrossRef]

T. T. L. Kristensen, W. Withayachumnankul, P. U. Jepsen, and D. Abbott, “Modeling terahertz heating effects on water,” Opt. Express18(5), 4727–4739 (2010).
[CrossRef] [PubMed]

H. T. Wang, B. Choi, and M. S. Tang, “Melanocytes are deficient in repair of oxidative DNA damage and UV-induced photoproducts,” Proc. Natl. Acad. Sci. U.S.A.107(27), 12180–12185 (2010).
[CrossRef] [PubMed]

2009 (4)

D. Menendez, A. Inga, and M. A. Resnick, “The expanding universe of p53 targets,” Nat. Rev. Cancer9(10), 724–737 (2009).
[CrossRef] [PubMed]

E. Bolderson, D. J. Richard, B. B. Zhou, and K. K. Khanna, “Recent advances in cancer therapy targeting proteins involved in DNA double-strand break repair,” Clin. Cancer Res.15(20), 6314–6320 (2009).
[CrossRef] [PubMed]

P. C. Ashworth, E. Pickwell-MacPherson, E. Provenzano, S. E. Pinder, A. D. Purushotham, M. Pepper, and V. P. Wallace, “Terahertz pulsed spectroscopy of freshly excised human breast cancer,” Opt. Express17(15), 12444–12454 (2009).
[CrossRef] [PubMed]

B. L. Mahaney, K. Meek, and S. P. Lees-Miller, “Repair of ionizing radiation-induced DNA double-strand breaks by non-homologous end-joining,” Biochem. J.417(3), 639–650 (2009).
[CrossRef] [PubMed]

2008 (4)

S. J. Kim, B. Born, M. Havenith, and M. Gruebele, “Real-time detection of protein-water dynamics upon protein folding by terahertz absorption spectroscopy,” Angew. Chem. Int. Ed. Engl.47(34), 6486–6489 (2008).
[CrossRef] [PubMed]

A. G. Markelz, “Terahertz Dielectric Sensitivity to Biomolecular Structure and Function,” IEEE J. Sel. Top. Quantum Electron.14(1), 180–190 (2008).
[CrossRef]

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] [PubMed]

W. M. Bonner, C. E. Redon, J. S. Dickey, A. J. Nakamura, O. A. Sedelnikova, S. Solier, and Y. Pommier, “γH2AX and cancer,” Nat. Rev. Cancer8(12), 957–967 (2008).
[CrossRef] [PubMed]

2007 (2)

O. A. Sedelnikova, A. Nakamura, O. Kovalchuk, I. Koturbash, S. A. Mitchell, S. A. Marino, D. J. Brenner, and W. M. Bonner, “DNA double-strand breaks form in bystander cells after microbeam irradiation of three-dimensional human tissue models,” Cancer Res.67(9), 4295–4302 (2007).
[CrossRef] [PubMed]

M. Tonouchi, “Cutting-edge terahertz technology,” Nat. Photonics1(2), 97–105 (2007).
[CrossRef]

2006 (3)

A. J. Fitzgerald, V. P. Wallace, M. Jimenez-Linan, L. Bobrow, R. J. Pye, A. D. Purushotham, and D. D. Arnone, “Terahertz pulsed imaging of human breast tumors,” Radiology239(2), 533–540 (2006).
[CrossRef] [PubMed]

S. M. Chitanvis, “Can low-power electromagnetic radiation disrupt hydrogen bonds in dsDNA?” J. Polym. Sci., B, Polym. Phys.44(18), 2740–2747 (2006).
[CrossRef]

J. Fillingham, M.-C. Keogh, and N. J. Krogan, “γH2AX and its role in DNA double-strand break repair,” Biochem. Cell Biol.84(4), 568–577 (2006).
[CrossRef] [PubMed]

2005 (3)

J. Cadet, E. Sage, and T. Douki, “Ultraviolet radiation-mediated damage to cellular DNA,” Mutat. Res.571(1-2), 3–17 (2005).
[CrossRef] [PubMed]

A. Krones-Herzig, S. Mittal, K. Yule, H. Liang, C. English, R. Urcis, T. Soni, E. D. Adamson, and D. Mercola, “Early growth response 1 acts as a tumor suppressor in vivo and in vitro via regulation of p53,” Cancer Res.65(12), 5133–5143 (2005).
[CrossRef] [PubMed]

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2004 (3)

D. Zimdars and J. S. White, “Terahertz reflection imaging for package and personnel inspection,” Proc. SPIE5411, 78–83 (2004).
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2003 (3)

O. A. Sedelnikova, D. R. Pilch, C. Redon, and W. M. Bonner, “Histone H2AX in DNA damage and repair,” Cancer Biol. Ther.2(3), 233–235 (2003).
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R. M. Woodward, V. P. Wallace, D. D. Arnone, E. H. Linfield, and M. Pepper, “Terahertz pulsed imaging of skin cancer in the time and frequency domain,” J. Biol. Phys.29(2/3), 257–259 (2003).
[CrossRef] [PubMed]

E. Berry, G. C. Walker, A. J. Fitzgerald, N. N. Zinov’ev, M. Chamberlain, S. W. Smye, R. E. Miles, and M. A. Smith, “Do in vivo terahertz imaging systems comply with safety guidelines?” J. Laser Appl.15(3), 192–198 (2003).
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2002 (5)

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[CrossRef] [PubMed]

A. G. Markelz, S. Whitmire, J. Hillebrecht, and R. Birge, “THz time domain spectroscopy of biomolecular conformational modes,” Phys. Med. Biol.47(21), 3797–3805 (2002).
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B. M. Fischer, M. Walther, and P. U. Jepsen, “Far-infrared vibrational modes of DNA components studied by terahertz time-domain spectroscopy,” Phys. Med. Biol.47(21), 3807–3814 (2002).
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2001 (4)

S. W. Smye, J. M. Chamberlain, A. J. Fitzgerald, and E. Berry, “The interaction between Terahertz radiation and biological tissue,” Phys. Med. Biol.46(9), R101–R112 (2001).
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S. Q. Wang, R. Setlow, M. Berwick, D. Polsky, A. A. Marghoob, A. W. Kopf, and R. S. Bart, “Ultraviolet A and melanoma: a review,” J. Am. Acad. Dermatol.44(5), 837–846 (2001).
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2000 (3)

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1998 (1)

E. P. Rogakou, D. R. Pilch, A. H. Orr, V. S. Ivanova, and W. M. Bonner, “DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139,” J. Biol. Chem.273(10), 5858–5868 (1998).
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1995 (1)

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1990 (1)

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Abbott, D.

Adamson, E. D.

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Agar, N. S.

N. S. Agar, G. M. Halliday, R. S. Barnetson, H. N. Ananthaswamy, M. Wheeler, and A. M. Jones, “The basal layer in human squamous tumors harbors more UVA than UVB fingerprint mutations: a role for UVA in human skin carcinogenesis,” Proc. Natl. Acad. Sci. U.S.A.101(14), 4954–4959 (2004).
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B. S. Alexandrov, K. Ø. Rasmussen, A. R. Bishop, A. Usheva, L. B. Alexandrov, S. Chong, Y. Dagon, L. G. Booshehri, C. H. Mielke, M. L. Phipps, J. S. Martinez, H.-T. Chen, and G. Rodriguez, “Non-thermal effects of terahertz radiation on gene expression in mouse stem cells,” Biomed. Opt. Express2(9), 2679–2689 (2011).
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B. S. Alexandrov, V. Gelev, A. R. Bishop, A. Usheva, and K. O. Rasmussen, “DNA breathing dynamics in the presence of a terahertz field,” Phys. Lett. A374(10), 1214–1217 (2010).
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J. Bock, Y. Fukuyo, S. Kang, M. L. Phipps, L. B. Alexandrov, K. Ø. Rasmussen, A. R. Bishop, E. D. Rosen, J. S. Martinez, H.-T. Chen, G. Rodriguez, B. S. Alexandrov, and A. Usheva, “Mammalian stem cells reprogramming in response to terahertz radiation,” PLoS ONE5(12), e15806 (2010).
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Alexandrov, L. B.

B. S. Alexandrov, K. Ø. Rasmussen, A. R. Bishop, A. Usheva, L. B. Alexandrov, S. Chong, Y. Dagon, L. G. Booshehri, C. H. Mielke, M. L. Phipps, J. S. Martinez, H.-T. Chen, and G. Rodriguez, “Non-thermal effects of terahertz radiation on gene expression in mouse stem cells,” Biomed. Opt. Express2(9), 2679–2689 (2011).
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J. Bock, Y. Fukuyo, S. Kang, M. L. Phipps, L. B. Alexandrov, K. Ø. Rasmussen, A. R. Bishop, E. D. Rosen, J. S. Martinez, H.-T. Chen, G. Rodriguez, B. S. Alexandrov, and A. Usheva, “Mammalian stem cells reprogramming in response to terahertz radiation,” PLoS ONE5(12), e15806 (2010).
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Altamirano, A.

J. S. Dickey, F. J. Zemp, A. Altamirano, O. A. Sedelnikova, W. M. Bonner, and O. Kovalchuk, “H2AX phosphorylation in response to DNA double-strand break formation during bystander signalling: effect of microRNA knockdown,” Radiat. Prot. Dosimetry143(2-4), 264–269 (2011).
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O. Kovalchuk, F. J. Zemp, J. N. Filkowski, A. M. Altamirano, J. S. Dickey, G. Jenkins-Baker, S. A. Marino, D. J. Brenner, W. M. Bonner, and O. A. Sedelnikova, “microRNAome changes in bystander three-dimensional human tissue models suggest priming of apoptotic pathways,” Carcinogenesis31(10), 1882–1888 (2010).
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Y. Zwang, A. Sas-Chen, Y. Drier, T. Shay, R. Avraham, M. Lauriola, E. Shema, E. Lidor-Nili, J. Jacob-Hirsch, N. Amariglio, Y. Lu, G. B. Mills, G. Rechavi, M. Oren, E. Domany, and Y. Yarden, “Two phases of mitogenic signaling unveil roles for p53 and EGR1 in elimination of inconsistent growth signals,” Mol. Cell42(4), 524–535 (2011).
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Ananthaswamy, H. N.

N. S. Agar, G. M. Halliday, R. S. Barnetson, H. N. Ananthaswamy, M. Wheeler, and A. M. Jones, “The basal layer in human squamous tumors harbors more UVA than UVB fingerprint mutations: a role for UVA in human skin carcinogenesis,” Proc. Natl. Acad. Sci. U.S.A.101(14), 4954–4959 (2004).
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Anderson, J. A.

P. Reynolds, J. A. Anderson, J. V. Harper, M. A. Hill, S. W. Botchway, A. W. Parker, and P. O’Neill, “The dynamics of Ku70/80 and DNA-PKcs at DSBs induced by ionizing radiation is dependent on the complexity of damage,” Nucleic Acids Res.40(21), 10821–10831 (2012).
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Arnone, D. D.

A. J. Fitzgerald, V. P. Wallace, M. Jimenez-Linan, L. Bobrow, R. J. Pye, A. D. Purushotham, and D. D. Arnone, “Terahertz pulsed imaging of human breast tumors,” Radiology239(2), 533–540 (2006).
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R. M. Woodward, V. P. Wallace, D. D. Arnone, E. H. Linfield, and M. Pepper, “Terahertz pulsed imaging of skin cancer in the time and frequency domain,” J. Biol. Phys.29(2/3), 257–259 (2003).
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Avraham, R.

Y. Zwang, A. Sas-Chen, Y. Drier, T. Shay, R. Avraham, M. Lauriola, E. Shema, E. Lidor-Nili, J. Jacob-Hirsch, N. Amariglio, Y. Lu, G. B. Mills, G. Rechavi, M. Oren, E. Domany, and Y. Yarden, “Two phases of mitogenic signaling unveil roles for p53 and EGR1 in elimination of inconsistent growth signals,” Mol. Cell42(4), 524–535 (2011).
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F. Blanchard, G. Sharma, L. Razzari, X. Ropagnol, H.-C. Bandulet, F. Vidal, R. Morandotti, J.-C. Kieffer, T. Ozaki, H. Tiedje, H. Haugen, M. Reid, and F. A. Hegmann, “Generation of intense terahertz radiation via optical methods,” IEEE J. Sel. Top. Quantum Electron.17(1), 5–16 (2011).
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Bao, Y.

H. Chen, Y. Bao, L. Yu, R. Jia, W. Cheng, and C. Shao, “Comparison of cellular damage response to low-dose-rate 125I seed irradiation and high-dose-rate gamma irradiation in human lung cancer cells,” Brachytherapy11(2), 149–156 (2012).
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Barat, R.

J. F. Federici, B. Schulkin, F. Huang, D. Gary, R. Barat, F. Oliveira, and D. Zimdars, “THz imaging and sensing for security applications: explosives, weapons and drugs,” Semicond. Sci. Technol.20(7), S266–S280 (2005).
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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).
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N. S. Agar, G. M. Halliday, R. S. Barnetson, H. N. Ananthaswamy, M. Wheeler, and A. M. Jones, “The basal layer in human squamous tumors harbors more UVA than UVB fingerprint mutations: a role for UVA in human skin carcinogenesis,” Proc. Natl. Acad. Sci. U.S.A.101(14), 4954–4959 (2004).
[CrossRef] [PubMed]

Bart, R. S.

S. Q. Wang, R. Setlow, M. Berwick, D. Polsky, A. A. Marghoob, A. W. Kopf, and R. S. Bart, “Ultraviolet A and melanoma: a review,” J. Am. Acad. Dermatol.44(5), 837–846 (2001).
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G. J. Wilmink, B. L. Ibey, C. L. Roth, R. L. Vincelette, B. D. Rivest, C. B. Horn, J. Bernhard, D. Roberson, and W. P. Roach, “Determination of death thresholds and identification of terahertz (THz) – specific gene expression signatures,” Proc. SPIE7562, 75620K, 75620K-8 (2010).
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G. J. Wilmink, B. D. Rivest, B. L. Ibey, C. L. Roth, J. Bernhard, and W. P. Roach, “Quantitative investigation of bioeffects associated with terahertz radiation,” Proc. SPIE7562, 75620L, 75620L-10 (2010).
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E. Berry, G. C. Walker, A. J. Fitzgerald, N. N. Zinov’ev, M. Chamberlain, S. W. Smye, R. E. Miles, and M. A. Smith, “Do in vivo terahertz imaging systems comply with safety guidelines?” J. Laser Appl.15(3), 192–198 (2003).
[CrossRef]

A. J. Fitzgerald, E. Berry, N. N. Zinovev, G. C. Walker, M. A. Smith, and J. M. Chamberlain, “An introduction to medical imaging with coherent terahertz frequency radiation,” Phys. Med. Biol.47(7), R67–R84 (2002).
[CrossRef] [PubMed]

S. W. Smye, J. M. Chamberlain, A. J. Fitzgerald, and E. Berry, “The interaction between Terahertz radiation and biological tissue,” Phys. Med. Biol.46(9), R101–R112 (2001).
[CrossRef] [PubMed]

Berwick, M.

S. Q. Wang, R. Setlow, M. Berwick, D. Polsky, A. A. Marghoob, A. W. Kopf, and R. S. Bart, “Ultraviolet A and melanoma: a review,” J. Am. Acad. Dermatol.44(5), 837–846 (2001).
[CrossRef] [PubMed]

Birge, R.

A. G. Markelz, S. Whitmire, J. Hillebrecht, and R. Birge, “THz time domain spectroscopy of biomolecular conformational modes,” Phys. Med. Biol.47(21), 3797–3805 (2002).
[CrossRef] [PubMed]

Bishop, A. R.

B. S. Alexandrov, K. Ø. Rasmussen, A. R. Bishop, A. Usheva, L. B. Alexandrov, S. Chong, Y. Dagon, L. G. Booshehri, C. H. Mielke, M. L. Phipps, J. S. Martinez, H.-T. Chen, and G. Rodriguez, “Non-thermal effects of terahertz radiation on gene expression in mouse stem cells,” Biomed. Opt. Express2(9), 2679–2689 (2011).
[CrossRef] [PubMed]

J. Bock, Y. Fukuyo, S. Kang, M. L. Phipps, L. B. Alexandrov, K. Ø. Rasmussen, A. R. Bishop, E. D. Rosen, J. S. Martinez, H.-T. Chen, G. Rodriguez, B. S. Alexandrov, and A. Usheva, “Mammalian stem cells reprogramming in response to terahertz radiation,” PLoS ONE5(12), e15806 (2010).
[CrossRef] [PubMed]

B. S. Alexandrov, V. Gelev, A. R. Bishop, A. Usheva, and K. O. Rasmussen, “DNA breathing dynamics in the presence of a terahertz field,” Phys. Lett. A374(10), 1214–1217 (2010).
[CrossRef] [PubMed]

Blanchard, F.

F. Blanchard, G. Sharma, L. Razzari, X. Ropagnol, H.-C. Bandulet, F. Vidal, R. Morandotti, J.-C. Kieffer, T. Ozaki, H. Tiedje, H. Haugen, M. Reid, and F. A. Hegmann, “Generation of intense terahertz radiation via optical methods,” IEEE J. Sel. Top. Quantum Electron.17(1), 5–16 (2011).
[CrossRef]

Bobrow, L.

A. J. Fitzgerald, V. P. Wallace, M. Jimenez-Linan, L. Bobrow, R. J. Pye, A. D. Purushotham, and D. D. Arnone, “Terahertz pulsed imaging of human breast tumors,” Radiology239(2), 533–540 (2006).
[CrossRef] [PubMed]

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J. Bock, Y. Fukuyo, S. Kang, M. L. Phipps, L. B. Alexandrov, K. Ø. Rasmussen, A. R. Bishop, E. D. Rosen, J. S. Martinez, H.-T. Chen, G. Rodriguez, B. S. Alexandrov, and A. Usheva, “Mammalian stem cells reprogramming in response to terahertz radiation,” PLoS ONE5(12), e15806 (2010).
[CrossRef] [PubMed]

Boelsma, E.

E. Boelsma, S. Gibbs, C. Faller, and M. Ponec, “Characterization and comparison of reconstructed skin models: morphological and immunohistochemical evaluation,” Acta Derm. Venereol.80(2), 82–88 (2000).
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E. Bolderson, D. J. Richard, B. B. Zhou, and K. K. Khanna, “Recent advances in cancer therapy targeting proteins involved in DNA double-strand break repair,” Clin. Cancer Res.15(20), 6314–6320 (2009).
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J. S. Dickey, F. J. Zemp, A. Altamirano, O. A. Sedelnikova, W. M. Bonner, and O. Kovalchuk, “H2AX phosphorylation in response to DNA double-strand break formation during bystander signalling: effect of microRNA knockdown,” Radiat. Prot. Dosimetry143(2-4), 264–269 (2011).
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O. Kovalchuk, F. J. Zemp, J. N. Filkowski, A. M. Altamirano, J. S. Dickey, G. Jenkins-Baker, S. A. Marino, D. J. Brenner, W. M. Bonner, and O. A. Sedelnikova, “microRNAome changes in bystander three-dimensional human tissue models suggest priming of apoptotic pathways,” Carcinogenesis31(10), 1882–1888 (2010).
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W. M. Bonner, C. E. Redon, J. S. Dickey, A. J. Nakamura, O. A. Sedelnikova, S. Solier, and Y. Pommier, “γH2AX and cancer,” Nat. Rev. Cancer8(12), 957–967 (2008).
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O. A. Sedelnikova, A. Nakamura, O. Kovalchuk, I. Koturbash, S. A. Mitchell, S. A. Marino, D. J. Brenner, and W. M. Bonner, “DNA double-strand breaks form in bystander cells after microbeam irradiation of three-dimensional human tissue models,” Cancer Res.67(9), 4295–4302 (2007).
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O. A. Sedelnikova, D. R. Pilch, C. Redon, and W. M. Bonner, “Histone H2AX in DNA damage and repair,” Cancer Biol. Ther.2(3), 233–235 (2003).
[CrossRef] [PubMed]

E. P. Rogakou, D. R. Pilch, A. H. Orr, V. S. Ivanova, and W. M. Bonner, “DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139,” J. Biol. Chem.273(10), 5858–5868 (1998).
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Booshehri, L. G.

Born, B.

S. J. Kim, B. Born, M. Havenith, and M. Gruebele, “Real-time detection of protein-water dynamics upon protein folding by terahertz absorption spectroscopy,” Angew. Chem. Int. Ed. Engl.47(34), 6486–6489 (2008).
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Bosserhoff, A.

M. Nagel, P. Haring Bolivar, M. Brucherseifer, H. Kurz, A. Bosserhoff, and R. Büttner, “Integrated THz technology for label-free genetic diagnostics,” Appl. Phys. Lett.80(1), 154–156 (2002).
[CrossRef]

M. Brucherseifer, M. Nagel, P. Haring Bolivar, H. Kurz, A. Bosserhoff, and R. Büttner, “Label-free probing of the binding state of DNA by time-domain terahertz sensing,” Appl. Phys. Lett.77(24), 4049–4051 (2000).
[CrossRef]

Botchway, S. W.

P. Reynolds, J. A. Anderson, J. V. Harper, M. A. Hill, S. W. Botchway, A. W. Parker, and P. O’Neill, “The dynamics of Ku70/80 and DNA-PKcs at DSBs induced by ionizing radiation is dependent on the complexity of damage,” Nucleic Acids Res.40(21), 10821–10831 (2012).
[CrossRef] [PubMed]

Brenner, D. J.

O. Kovalchuk, F. J. Zemp, J. N. Filkowski, A. M. Altamirano, J. S. Dickey, G. Jenkins-Baker, S. A. Marino, D. J. Brenner, W. M. Bonner, and O. A. Sedelnikova, “microRNAome changes in bystander three-dimensional human tissue models suggest priming of apoptotic pathways,” Carcinogenesis31(10), 1882–1888 (2010).
[CrossRef] [PubMed]

O. A. Sedelnikova, A. Nakamura, O. Kovalchuk, I. Koturbash, S. A. Mitchell, S. A. Marino, D. J. Brenner, and W. M. Bonner, “DNA double-strand breaks form in bystander cells after microbeam irradiation of three-dimensional human tissue models,” Cancer Res.67(9), 4295–4302 (2007).
[CrossRef] [PubMed]

Brucherseifer, M.

M. Nagel, P. Haring Bolivar, M. Brucherseifer, H. Kurz, A. Bosserhoff, and R. Büttner, “Integrated THz technology for label-free genetic diagnostics,” Appl. Phys. Lett.80(1), 154–156 (2002).
[CrossRef]

M. Brucherseifer, M. Nagel, P. Haring Bolivar, H. Kurz, A. Bosserhoff, and R. Büttner, “Label-free probing of the binding state of DNA by time-domain terahertz sensing,” Appl. Phys. Lett.77(24), 4049–4051 (2000).
[CrossRef]

Büttner, R.

M. Nagel, P. Haring Bolivar, M. Brucherseifer, H. Kurz, A. Bosserhoff, and R. Büttner, “Integrated THz technology for label-free genetic diagnostics,” Appl. Phys. Lett.80(1), 154–156 (2002).
[CrossRef]

M. Brucherseifer, M. Nagel, P. Haring Bolivar, H. Kurz, A. Bosserhoff, and R. Büttner, “Label-free probing of the binding state of DNA by time-domain terahertz sensing,” Appl. Phys. Lett.77(24), 4049–4051 (2000).
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J. Cadet, E. Sage, and T. Douki, “Ultraviolet radiation-mediated damage to cellular DNA,” Mutat. Res.571(1-2), 3–17 (2005).
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A. J. Fitzgerald, E. Berry, N. N. Zinovev, G. C. Walker, M. A. Smith, and J. M. Chamberlain, “An introduction to medical imaging with coherent terahertz frequency radiation,” Phys. Med. Biol.47(7), R67–R84 (2002).
[CrossRef] [PubMed]

S. W. Smye, J. M. Chamberlain, A. J. Fitzgerald, and E. Berry, “The interaction between Terahertz radiation and biological tissue,” Phys. Med. Biol.46(9), R101–R112 (2001).
[CrossRef] [PubMed]

Chamberlain, M.

E. Berry, G. C. Walker, A. J. Fitzgerald, N. N. Zinov’ev, M. Chamberlain, S. W. Smye, R. E. Miles, and M. A. Smith, “Do in vivo terahertz imaging systems comply with safety guidelines?” J. Laser Appl.15(3), 192–198 (2003).
[CrossRef]

Chen, H.

H. Chen, Y. Bao, L. Yu, R. Jia, W. Cheng, and C. Shao, “Comparison of cellular damage response to low-dose-rate 125I seed irradiation and high-dose-rate gamma irradiation in human lung cancer cells,” Brachytherapy11(2), 149–156 (2012).
[CrossRef] [PubMed]

Chen, H.-T.

B. S. Alexandrov, K. Ø. Rasmussen, A. R. Bishop, A. Usheva, L. B. Alexandrov, S. Chong, Y. Dagon, L. G. Booshehri, C. H. Mielke, M. L. Phipps, J. S. Martinez, H.-T. Chen, and G. Rodriguez, “Non-thermal effects of terahertz radiation on gene expression in mouse stem cells,” Biomed. Opt. Express2(9), 2679–2689 (2011).
[CrossRef] [PubMed]

J. Bock, Y. Fukuyo, S. Kang, M. L. Phipps, L. B. Alexandrov, K. Ø. Rasmussen, A. R. Bishop, E. D. Rosen, J. S. Martinez, H.-T. Chen, G. Rodriguez, B. S. Alexandrov, and A. Usheva, “Mammalian stem cells reprogramming in response to terahertz radiation,” PLoS ONE5(12), e15806 (2010).
[CrossRef] [PubMed]

Cheng, W.

H. Chen, Y. Bao, L. Yu, R. Jia, W. Cheng, and C. Shao, “Comparison of cellular damage response to low-dose-rate 125I seed irradiation and high-dose-rate gamma irradiation in human lung cancer cells,” Brachytherapy11(2), 149–156 (2012).
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S. M. Chitanvis, “Can low-power electromagnetic radiation disrupt hydrogen bonds in dsDNA?” J. Polym. Sci., B, Polym. Phys.44(18), 2740–2747 (2006).
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H. T. Wang, B. Choi, and M. S. Tang, “Melanocytes are deficient in repair of oxidative DNA damage and UV-induced photoproducts,” Proc. Natl. Acad. Sci. U.S.A.107(27), 12180–12185 (2010).
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P. U. Jepsen, D. G. Cooke, and M. Koch, “Terahertz spectroscopy and imaging — Modern techniques and applications,” Laser Photonics Rev.5(1), 124–166 (2011).
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K. K. Khanna and S. P. Jackson, “DNA double-strand breaks: signaling, repair and the cancer connection,” Nat. Genet.27(3), 247–254 (2001).
[CrossRef] [PubMed]

Nat. Photonics (1)

M. Tonouchi, “Cutting-edge terahertz technology,” Nat. Photonics1(2), 97–105 (2007).
[CrossRef]

Nat. Rev. Cancer (2)

D. Menendez, A. Inga, and M. A. Resnick, “The expanding universe of p53 targets,” Nat. Rev. Cancer9(10), 724–737 (2009).
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W. M. Bonner, C. E. Redon, J. S. Dickey, A. J. Nakamura, O. A. Sedelnikova, S. Solier, and Y. Pommier, “γH2AX and cancer,” Nat. Rev. Cancer8(12), 957–967 (2008).
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Nat. Rev. Mol. Cell Biol. (2)

P. McGlynn and R. G. Lloyd, “Recombinational repair and restart of damaged replication forks,” Nat. Rev. Mol. Cell Biol.3(11), 859–870 (2002).
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T. Sperka, J. Wang, and K. L. Rudolph, “DNA damage checkpoints in stem cells, ageing and cancer,” Nat. Rev. Mol. Cell Biol.13(9), 579–590 (2012).
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Nature (1)

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Nucleic Acids Res. (1)

P. Reynolds, J. A. Anderson, J. V. Harper, M. A. Hill, S. W. Botchway, A. W. Parker, and P. O’Neill, “The dynamics of Ku70/80 and DNA-PKcs at DSBs induced by ionizing radiation is dependent on the complexity of damage,” Nucleic Acids Res.40(21), 10821–10831 (2012).
[CrossRef] [PubMed]

Opt. Express (2)

Photodermatol. Photoimmunol. Photomed. (1)

S. Seité, D. Moyal, M. P. Verdier, C. Hourseau, and A. Fourtanier, “Accumulated p53 protein and UVA protection level of sunscreens,” Photodermatol. Photoimmunol. Photomed.16(1), 3–9 (2000).
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Phys. Lett. A (1)

B. S. Alexandrov, V. Gelev, A. R. Bishop, A. Usheva, and K. O. Rasmussen, “DNA breathing dynamics in the presence of a terahertz field,” Phys. Lett. A374(10), 1214–1217 (2010).
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Phys. Med. Biol. (4)

A. J. Fitzgerald, E. Berry, N. N. Zinovev, G. C. Walker, M. A. Smith, and J. M. Chamberlain, “An introduction to medical imaging with coherent terahertz frequency radiation,” Phys. Med. Biol.47(7), R67–R84 (2002).
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A. G. Markelz, S. Whitmire, J. Hillebrecht, and R. Birge, “THz time domain spectroscopy of biomolecular conformational modes,” Phys. Med. Biol.47(21), 3797–3805 (2002).
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B. M. Fischer, M. Walther, and P. U. Jepsen, “Far-infrared vibrational modes of DNA components studied by terahertz time-domain spectroscopy,” Phys. Med. Biol.47(21), 3807–3814 (2002).
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S. W. Smye, J. M. Chamberlain, A. J. Fitzgerald, and E. Berry, “The interaction between Terahertz radiation and biological tissue,” Phys. Med. Biol.46(9), R101–R112 (2001).
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Phys. Rev. A (1)

W. Zhuang, Y. Feng, and E. W. Prohofsky, “Self-consistent calculation of localized DNA vibrational properties at a double-helix-single-strand junction with anharmonic potential,” Phys. Rev. A41(12), 7033–7042 (1990).
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PLoS ONE (1)

J. Bock, Y. Fukuyo, S. Kang, M. L. Phipps, L. B. Alexandrov, K. Ø. Rasmussen, A. R. Bishop, E. D. Rosen, J. S. Martinez, H.-T. Chen, G. Rodriguez, B. S. Alexandrov, and A. Usheva, “Mammalian stem cells reprogramming in response to terahertz radiation,” PLoS ONE5(12), e15806 (2010).
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Proc. Natl. Acad. Sci. U.S.A. (2)

N. S. Agar, G. M. Halliday, R. S. Barnetson, H. N. Ananthaswamy, M. Wheeler, and A. M. Jones, “The basal layer in human squamous tumors harbors more UVA than UVB fingerprint mutations: a role for UVA in human skin carcinogenesis,” Proc. Natl. Acad. Sci. U.S.A.101(14), 4954–4959 (2004).
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H. T. Wang, B. Choi, and M. S. Tang, “Melanocytes are deficient in repair of oxidative DNA damage and UV-induced photoproducts,” Proc. Natl. Acad. Sci. U.S.A.107(27), 12180–12185 (2010).
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Proc. SPIE (3)

G. J. Wilmink, B. L. Ibey, C. L. Roth, R. L. Vincelette, B. D. Rivest, C. B. Horn, J. Bernhard, D. Roberson, and W. P. Roach, “Determination of death thresholds and identification of terahertz (THz) – specific gene expression signatures,” Proc. SPIE7562, 75620K, 75620K-8 (2010).
[CrossRef]

G. J. Wilmink, B. D. Rivest, B. L. Ibey, C. L. Roth, J. Bernhard, and W. P. Roach, “Quantitative investigation of bioeffects associated with terahertz radiation,” Proc. SPIE7562, 75620L, 75620L-10 (2010).
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D. Zimdars and J. S. White, “Terahertz reflection imaging for package and personnel inspection,” Proc. SPIE5411, 78–83 (2004).
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Radiat. Prot. Dosimetry (1)

J. S. Dickey, F. J. Zemp, A. Altamirano, O. A. Sedelnikova, W. M. Bonner, and O. Kovalchuk, “H2AX phosphorylation in response to DNA double-strand break formation during bystander signalling: effect of microRNA knockdown,” Radiat. Prot. Dosimetry143(2-4), 264–269 (2011).
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Radiat. Res. (2)

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] [PubMed]

H. Hintzsche, C. Jastrow, T. Kleine-Ostmann, H. Stopper, E. Schmid, and T. Schrader, “Terahertz radiation induces spindle disturbances in human-hamster hybrid cells,” Radiat. Res.175(5), 569–574 (2011).
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Radiology (1)

A. J. Fitzgerald, V. P. Wallace, M. Jimenez-Linan, L. Bobrow, R. J. Pye, A. D. Purushotham, and D. D. Arnone, “Terahertz pulsed imaging of human breast tumors,” Radiology239(2), 533–540 (2006).
[CrossRef] [PubMed]

Semicond. Sci. Technol. (1)

J. F. Federici, B. Schulkin, F. Huang, D. Gary, R. Barat, F. Oliveira, and D. Zimdars, “THz imaging and sensing for security applications: explosives, weapons and drugs,” Semicond. Sci. Technol.20(7), S266–S280 (2005).
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Other (3)

P. C. Ashworth, P. O’Kelly, A. D. Purushotham, S. E. Pinder, M. Kontos, M. Pepper, and V. P. Wallace, “An intra-operative THz probe for use during the surgical removal of breast tumors,” in 33rd International Conference on Infrared, Millimeter and Terahertz Waves, 2008. IRMMW-THz 2008 (2008), pp. 1–3. doi: 10.1109/ICIMW.2008.4665810.
[CrossRef]

“TeraView receives MHRA approval to conduct in-vivo cancer imaging trials,” http://www.teraview.com/news/terahertz-news/TeraView-receives-in-vivo-trials-approval.html

D. M. Mittleman, Sensing with Terahertz Radiation (Springer, 2010).

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Figures (4)

Fig. 1
Fig. 1

Exposure of artificial human skin tissues equivalents to intense THz pulses. (a) Schematic of the tilted-pulse-front THz pulse source and EpiDermFT tissue in a single-well insert placed at the focus of THz beam. (b) Waveform of a 1.0 μJ THz pulse and (c) corresponding amplitude spectrum. (d) Histology of the EpiDermFT tissue sample (400X image by MatTek Corporation, used with permission). The stained paraffin section reveals epidermis containing basal, spinous, granular keratinocytes and stratum corneum. The dermis contains numerous viable fibroblasts. (e) Image of the THz beam spot size at the sample location. The 1/e2 diameter of the THz beam is 1.5 mm. The dashed square shows the size of the area (2x2 mm2) that was cut out to separate exposed from unexposed tissue.

Fig. 2
Fig. 2

Induction of γH2AX in artificial human skin tissues equivalents following 10 minute exposure to either high (1.0 μJ) or low (0.1 μJ) energy THz pulses, or 2 minute exposure to UVA (400 nm) pulses (0.080 μJ), as compared to control (CT) samples. The pulse repetition rate was 1 kHz. Actin was used as a loading control. Each experiment included pooled lysates from three tissues for each exposure condition with equal representation for each tissue.

Fig. 3
Fig. 3

Confocal fluorescence images of tissue sample cross-sections showing the incidence of γH2AX foci (localized green spots). Blue spots indicate cell nuclei. γH2AX-harboring cells (markers for double strand breaks in DNA) inside cell nuclei appear as blue-green spots. Panels from left to right show representative images for control (CT), low THz pulse energy (0.1 μJ), high THz pulse energy (1.0 μJ), and UVA-exposed tissues. Scale bar is 100 μm.

Fig. 4
Fig. 4

Expression of tumor suppressor and cell cycle regulatory proteins in artificial human 3D skin tissues equivalents following 10 minute exposure to either high (1.0 μJ) or low (0.1 μJ) energy THz pulses, or two minute exposure to 0.080 μJ UVA (400 nm) pulses, as compared to unexposed control (CT) samples. Actin was used as a loading control.

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