Abstract

The apoptosis of cancer cells was experimentally measured by terahertz (THz) biosensors based on the metamaterials (MMs). The non-bianisotropic resonance with an electric field of up to 106 V/m was exhibited at 0.85 THz, where the magnetic dipoles were cancelled in the unit cell. The simulate results show the dependence of the frequency shift on the occupying ratio and refractive index of analytes. The theoretical sensitivity was calculated to 182 GHz/RIU. The experimental results imply that the resonant frequency would red shift with the increase of the concentration of cancer cells. Furthermore, the apoptosis of cancer cells HSC3 under the effect of drug concentration from 1 to 15 μM and drug action time from 24 to 72 hours were also studied by the biosensors, respectively. It shows that the trend agrees with the results measured by the biological CCK-8 kits method. Our proposed MMs-based biosensors may supply a novel viewpoint on cell apoptosis from a physical perspective and be a valuable complementary reference for biological study.

© 2018 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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References

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2017 (10)

K. Batrakov and S. Maksimenko, “Graphene layered systems as a terahertz source with tuned frequency,” Phys. Rev. B 95(20), 205408 (2017).
[Crossref]

N. T. Yardimci, S. Cakmakyapan, S. Hemmati, and M. Jarrahi, “A High-Power Broadband Terahertz Source Enabled by Three-Dimensional Light Confinement in a Plasmonic Nanocavity,” Sci. Rep. 7(1), 4166 (2017).
[Crossref] [PubMed]

I. Dey, K. Jana, V. Y. Fedorov, A. D. Koulouklidis, A. Mondal, M. Shaikh, D. Sarkar, A. D. Lad, S. Tzortzakis, A. Couairon, and G. R. Kumar, “Highly efficient broadband terahertz generation from ultrashort laser filamentation in liquids,” Nat. Commun. 8(1), 1184 (2017).
[Crossref] [PubMed]

W. Zhang, D. Nickel, and D. Mittleman, “High-pressure cell for terahertz time-domain spectroscopy,” Opt. Express 25(3), 2983–2993 (2017).
[Crossref]

L. Valzania, P. Zolliker, and E. Hack, “Topography of hidden objects using THz digital holography with multi-beam interferences,” Opt. Express 25(10), 11038–11047 (2017).
[Crossref] [PubMed]

Z. Li, W. Chen, F. Lian, H. Ge, and A. Guan, “Wavelength Selection Method Based on Differential Evolution for Precise Quantitative Analysis Using Terahertz Time-Domain Spectroscopy,” Appl. Spectrosc. 71(12), 2653–2660 (2017).
[Crossref] [PubMed]

H. Iwasaki, M. Nakamura, N. Komatsubara, M. Okano, M. Nakasako, H. Sato, and S. Watanabe, “Controlled Terahertz Birefringence in Stretched Poly(lactic acid) Films Investigated by Terahertz Time-Domain Spectroscopy and Wide-Angle X-ray Scattering,” J. Phys. Chem. B 121(28), 6951–6957 (2017).
[Crossref] [PubMed]

L. H. Du, J. Li, Q. Liu, J. H. Zhao, and L. G. Zhu, “High-Q Fano-like resonance based on a symmetric dimer structure and its terahertz sensing application,” Opt. Mater. Express 7(4), 1335–1342 (2017).
[Crossref]

R. Xia, X. Jing, X. Gui, Y. Tian, and Z. Hong, “Broadband terahertz half-wave plate based on anisotropic polarization conversion metamaterials,” Opt. Mater. Express 7(3), 977–988 (2017).
[Crossref]

D. Wei, C. Harris, and S. Law, “Volume plasmon polaritons in semiconductor hyperbolic metamaterials,” Opt. Mater. Express 7(7), 2672–2681 (2017).
[Crossref]

2016 (1)

C. Zhang, L. Liang, L. Ding, B. Jin, Y. Hou, C. Li, L. Jiang, W. Liu, W. Hu, Y. Lu, L. Kang, W. Xu, J. Chen, and P. Wu, “Label-free measurements on cell apoptosis using a terahertz metamaterial-based biosensor,” Appl. Phys. Lett. 108(24), 241105 (2016).
[Crossref]

2015 (2)

R. L. Siegel, K. D. Miller, and A. Jemal, “Cancer Statistics, 2015,” CA Cancer J. Clin. 65(1), 5–29 (2015).
[Crossref] [PubMed]

L. Cong, S. Tan, R. Yahiaoui, F. Yan, W. Zhang, and R. Singh, “Experimental demonstration of ultrasensitive sensing with terahertz metamaterial absorbers: A comparison with the metasurfaces,” Appl. Phys. Lett. 106(3), 031107 (2015).
[Crossref]

2014 (3)

N. Yu and F. Capasso, “Flat optics with designer metasurfaces,” Nat. Mater. 13(2), 139–150 (2014).
[Crossref] [PubMed]

S.-L. Chen, Y.-C. Chang, C. Zhang, J. G. Ok, T. Ling, M. T. Mihnev, T. B. Norris, and L. J. Guo, “Efficient real-time detection of terahertz pulse radiation based on photoacoustic conversion by carbon nanotube nanocomposite,” Nat. Photonics 8(7), 537–542 (2014).
[Crossref]

A. Kamal, S. Faazil, and M. S. Malik, “Apoptosis-inducing agents: A patent review (2010 - 2013),” Expert Opin. Ther. Pat. 24(3), 339–354 (2014).
[Crossref] [PubMed]

2013 (4)

C. Seco-Martorell, V. López-Domínguez, G. Arauz-Garofalo, A. Redo-Sanchez, J. Palacios, and J. Tejada, “Goya’s artwork imaging with Terahertz waves,” Opt. Express 21(15), 17800–17805 (2013).
[Crossref] [PubMed]

J. Wang, C. Fan, J. He, P. Ding, E. Liang, and Q. Xue, “Double Fano resonances due to interplay of electric and magnetic plasmon modes in planar plasmonic structure with high sensing sensitivity,” Opt. Express 21(2), 2236–2244 (2013).
[Crossref] [PubMed]

C. Cao, J. Zhang, X. Wen, S. L. Dodson, N. T. Dao, L. M. Wong, S. Wang, S. Li, A. T. Phan, and Q. Xiong, “Metamaterials-Based Label-Free Nanosensor for Conformation and Affinity Biosensing,” ACS Nano 7(9), 7583–7591 (2013).
[Crossref] [PubMed]

A. Kaczmarek, P. Vandenabeele, and D. V. Krysko, “Necroptosis: The Release of Damage-Associated Molecular Patterns and Its Physiological Relevance,” Immunity 38(2), 209–223 (2013).
[Crossref] [PubMed]

2011 (2)

H. Tao, L. R. Chieffo, M. A. Brenckle, S. M. Siebert, M. Liu, A. C. Strikwerda, K. Fan, D. L. Kaplan, X. Zhang, R. D. Averitt, and F. G. Omenetto, “Metamaterials on Paper as a Sensing Platform,” Adv. Mater. 23(28), 3197–3201 (2011).
[Crossref] [PubMed]

N. Yu, P. Genevet, M. A. Kats, F. Aieta, J. P. Tetienne, F. Capasso, and Z. Gaburro, “Light propagation with phase discontinuities: generalized laws of reflection and refraction,” Science 334(6054), 333–337 (2011).
[Crossref] [PubMed]

2010 (1)

2007 (2)

W. J. Padilla, M. T. Aronsson, C. Highstrete, M. Lee, A. J. Taylor, and R. D. Averitt, “Electrically resonant terahertz metamaterials: Theoretical and experimental investigations,” Phys. Rev. B 75(4), 041102 (2007).
[Crossref]

H.-T. Chen, J. F. O’Hara, A. J. Taylor, R. D. Averitt, C. Highstrete, M. Lee, and W. J. Padilla, “Complementary planar terahertz metamaterials,” Opt. Express 15(3), 1084–1095 (2007).
[Crossref] [PubMed]

2005 (1)

B. Levine and J. Yuan, “Autophagy in cell death: An innocent convict?” J. Clin. Invest. 115(10), 2679–2688 (2005).
[Crossref] [PubMed]

2001 (1)

R. A. Shelby, D. R. Smith, and S. Schultz, “Experimental Verification of a Negative Index of Refraction,” Science 292(5514), 77–79 (2001).
[Crossref] [PubMed]

Aieta, F.

N. Yu, P. Genevet, M. A. Kats, F. Aieta, J. P. Tetienne, F. Capasso, and Z. Gaburro, “Light propagation with phase discontinuities: generalized laws of reflection and refraction,” Science 334(6054), 333–337 (2011).
[Crossref] [PubMed]

Arauz-Garofalo, G.

Aronsson, M. T.

W. J. Padilla, M. T. Aronsson, C. Highstrete, M. Lee, A. J. Taylor, and R. D. Averitt, “Electrically resonant terahertz metamaterials: Theoretical and experimental investigations,” Phys. Rev. B 75(4), 041102 (2007).
[Crossref]

Averitt, R. D.

H. Tao, L. R. Chieffo, M. A. Brenckle, S. M. Siebert, M. Liu, A. C. Strikwerda, K. Fan, D. L. Kaplan, X. Zhang, R. D. Averitt, and F. G. Omenetto, “Metamaterials on Paper as a Sensing Platform,” Adv. Mater. 23(28), 3197–3201 (2011).
[Crossref] [PubMed]

W. J. Padilla, M. T. Aronsson, C. Highstrete, M. Lee, A. J. Taylor, and R. D. Averitt, “Electrically resonant terahertz metamaterials: Theoretical and experimental investigations,” Phys. Rev. B 75(4), 041102 (2007).
[Crossref]

H.-T. Chen, J. F. O’Hara, A. J. Taylor, R. D. Averitt, C. Highstrete, M. Lee, and W. J. Padilla, “Complementary planar terahertz metamaterials,” Opt. Express 15(3), 1084–1095 (2007).
[Crossref] [PubMed]

Batrakov, K.

K. Batrakov and S. Maksimenko, “Graphene layered systems as a terahertz source with tuned frequency,” Phys. Rev. B 95(20), 205408 (2017).
[Crossref]

Brenckle, M. A.

H. Tao, L. R. Chieffo, M. A. Brenckle, S. M. Siebert, M. Liu, A. C. Strikwerda, K. Fan, D. L. Kaplan, X. Zhang, R. D. Averitt, and F. G. Omenetto, “Metamaterials on Paper as a Sensing Platform,” Adv. Mater. 23(28), 3197–3201 (2011).
[Crossref] [PubMed]

Cakmakyapan, S.

N. T. Yardimci, S. Cakmakyapan, S. Hemmati, and M. Jarrahi, “A High-Power Broadband Terahertz Source Enabled by Three-Dimensional Light Confinement in a Plasmonic Nanocavity,” Sci. Rep. 7(1), 4166 (2017).
[Crossref] [PubMed]

Cao, C.

C. Cao, J. Zhang, X. Wen, S. L. Dodson, N. T. Dao, L. M. Wong, S. Wang, S. Li, A. T. Phan, and Q. Xiong, “Metamaterials-Based Label-Free Nanosensor for Conformation and Affinity Biosensing,” ACS Nano 7(9), 7583–7591 (2013).
[Crossref] [PubMed]

Capasso, F.

N. Yu and F. Capasso, “Flat optics with designer metasurfaces,” Nat. Mater. 13(2), 139–150 (2014).
[Crossref] [PubMed]

N. Yu, P. Genevet, M. A. Kats, F. Aieta, J. P. Tetienne, F. Capasso, and Z. Gaburro, “Light propagation with phase discontinuities: generalized laws of reflection and refraction,” Science 334(6054), 333–337 (2011).
[Crossref] [PubMed]

Chang, Y.-C.

S.-L. Chen, Y.-C. Chang, C. Zhang, J. G. Ok, T. Ling, M. T. Mihnev, T. B. Norris, and L. J. Guo, “Efficient real-time detection of terahertz pulse radiation based on photoacoustic conversion by carbon nanotube nanocomposite,” Nat. Photonics 8(7), 537–542 (2014).
[Crossref]

Chen, H.-T.

Chen, J.

C. Zhang, L. Liang, L. Ding, B. Jin, Y. Hou, C. Li, L. Jiang, W. Liu, W. Hu, Y. Lu, L. Kang, W. Xu, J. Chen, and P. Wu, “Label-free measurements on cell apoptosis using a terahertz metamaterial-based biosensor,” Appl. Phys. Lett. 108(24), 241105 (2016).
[Crossref]

Chen, S.-L.

S.-L. Chen, Y.-C. Chang, C. Zhang, J. G. Ok, T. Ling, M. T. Mihnev, T. B. Norris, and L. J. Guo, “Efficient real-time detection of terahertz pulse radiation based on photoacoustic conversion by carbon nanotube nanocomposite,” Nat. Photonics 8(7), 537–542 (2014).
[Crossref]

Chen, W.

Chieffo, L. R.

H. Tao, L. R. Chieffo, M. A. Brenckle, S. M. Siebert, M. Liu, A. C. Strikwerda, K. Fan, D. L. Kaplan, X. Zhang, R. D. Averitt, and F. G. Omenetto, “Metamaterials on Paper as a Sensing Platform,” Adv. Mater. 23(28), 3197–3201 (2011).
[Crossref] [PubMed]

Cong, L.

L. Cong, S. Tan, R. Yahiaoui, F. Yan, W. Zhang, and R. Singh, “Experimental demonstration of ultrasensitive sensing with terahertz metamaterial absorbers: A comparison with the metasurfaces,” Appl. Phys. Lett. 106(3), 031107 (2015).
[Crossref]

Couairon, A.

I. Dey, K. Jana, V. Y. Fedorov, A. D. Koulouklidis, A. Mondal, M. Shaikh, D. Sarkar, A. D. Lad, S. Tzortzakis, A. Couairon, and G. R. Kumar, “Highly efficient broadband terahertz generation from ultrashort laser filamentation in liquids,” Nat. Commun. 8(1), 1184 (2017).
[Crossref] [PubMed]

Dao, N. T.

C. Cao, J. Zhang, X. Wen, S. L. Dodson, N. T. Dao, L. M. Wong, S. Wang, S. Li, A. T. Phan, and Q. Xiong, “Metamaterials-Based Label-Free Nanosensor for Conformation and Affinity Biosensing,” ACS Nano 7(9), 7583–7591 (2013).
[Crossref] [PubMed]

Dey, I.

I. Dey, K. Jana, V. Y. Fedorov, A. D. Koulouklidis, A. Mondal, M. Shaikh, D. Sarkar, A. D. Lad, S. Tzortzakis, A. Couairon, and G. R. Kumar, “Highly efficient broadband terahertz generation from ultrashort laser filamentation in liquids,” Nat. Commun. 8(1), 1184 (2017).
[Crossref] [PubMed]

Ding, L.

C. Zhang, L. Liang, L. Ding, B. Jin, Y. Hou, C. Li, L. Jiang, W. Liu, W. Hu, Y. Lu, L. Kang, W. Xu, J. Chen, and P. Wu, “Label-free measurements on cell apoptosis using a terahertz metamaterial-based biosensor,” Appl. Phys. Lett. 108(24), 241105 (2016).
[Crossref]

Ding, P.

Ding, Y. J.

Dodson, S. L.

C. Cao, J. Zhang, X. Wen, S. L. Dodson, N. T. Dao, L. M. Wong, S. Wang, S. Li, A. T. Phan, and Q. Xiong, “Metamaterials-Based Label-Free Nanosensor for Conformation and Affinity Biosensing,” ACS Nano 7(9), 7583–7591 (2013).
[Crossref] [PubMed]

Du, L. H.

Faazil, S.

A. Kamal, S. Faazil, and M. S. Malik, “Apoptosis-inducing agents: A patent review (2010 - 2013),” Expert Opin. Ther. Pat. 24(3), 339–354 (2014).
[Crossref] [PubMed]

Fan, C.

Fan, K.

H. Tao, L. R. Chieffo, M. A. Brenckle, S. M. Siebert, M. Liu, A. C. Strikwerda, K. Fan, D. L. Kaplan, X. Zhang, R. D. Averitt, and F. G. Omenetto, “Metamaterials on Paper as a Sensing Platform,” Adv. Mater. 23(28), 3197–3201 (2011).
[Crossref] [PubMed]

Fedorov, V. Y.

I. Dey, K. Jana, V. Y. Fedorov, A. D. Koulouklidis, A. Mondal, M. Shaikh, D. Sarkar, A. D. Lad, S. Tzortzakis, A. Couairon, and G. R. Kumar, “Highly efficient broadband terahertz generation from ultrashort laser filamentation in liquids,” Nat. Commun. 8(1), 1184 (2017).
[Crossref] [PubMed]

Gaburro, Z.

N. Yu, P. Genevet, M. A. Kats, F. Aieta, J. P. Tetienne, F. Capasso, and Z. Gaburro, “Light propagation with phase discontinuities: generalized laws of reflection and refraction,” Science 334(6054), 333–337 (2011).
[Crossref] [PubMed]

Ge, H.

Genevet, P.

N. Yu, P. Genevet, M. A. Kats, F. Aieta, J. P. Tetienne, F. Capasso, and Z. Gaburro, “Light propagation with phase discontinuities: generalized laws of reflection and refraction,” Science 334(6054), 333–337 (2011).
[Crossref] [PubMed]

Guan, A.

Gui, X.

Guo, L. J.

S.-L. Chen, Y.-C. Chang, C. Zhang, J. G. Ok, T. Ling, M. T. Mihnev, T. B. Norris, and L. J. Guo, “Efficient real-time detection of terahertz pulse radiation based on photoacoustic conversion by carbon nanotube nanocomposite,” Nat. Photonics 8(7), 537–542 (2014).
[Crossref]

Hack, E.

Harris, C.

He, J.

Hemmati, S.

N. T. Yardimci, S. Cakmakyapan, S. Hemmati, and M. Jarrahi, “A High-Power Broadband Terahertz Source Enabled by Three-Dimensional Light Confinement in a Plasmonic Nanocavity,” Sci. Rep. 7(1), 4166 (2017).
[Crossref] [PubMed]

Highstrete, C.

W. J. Padilla, M. T. Aronsson, C. Highstrete, M. Lee, A. J. Taylor, and R. D. Averitt, “Electrically resonant terahertz metamaterials: Theoretical and experimental investigations,” Phys. Rev. B 75(4), 041102 (2007).
[Crossref]

H.-T. Chen, J. F. O’Hara, A. J. Taylor, R. D. Averitt, C. Highstrete, M. Lee, and W. J. Padilla, “Complementary planar terahertz metamaterials,” Opt. Express 15(3), 1084–1095 (2007).
[Crossref] [PubMed]

Hong, Z.

Hou, Y.

C. Zhang, L. Liang, L. Ding, B. Jin, Y. Hou, C. Li, L. Jiang, W. Liu, W. Hu, Y. Lu, L. Kang, W. Xu, J. Chen, and P. Wu, “Label-free measurements on cell apoptosis using a terahertz metamaterial-based biosensor,” Appl. Phys. Lett. 108(24), 241105 (2016).
[Crossref]

Hu, W.

C. Zhang, L. Liang, L. Ding, B. Jin, Y. Hou, C. Li, L. Jiang, W. Liu, W. Hu, Y. Lu, L. Kang, W. Xu, J. Chen, and P. Wu, “Label-free measurements on cell apoptosis using a terahertz metamaterial-based biosensor,” Appl. Phys. Lett. 108(24), 241105 (2016).
[Crossref]

Iwasaki, H.

H. Iwasaki, M. Nakamura, N. Komatsubara, M. Okano, M. Nakasako, H. Sato, and S. Watanabe, “Controlled Terahertz Birefringence in Stretched Poly(lactic acid) Films Investigated by Terahertz Time-Domain Spectroscopy and Wide-Angle X-ray Scattering,” J. Phys. Chem. B 121(28), 6951–6957 (2017).
[Crossref] [PubMed]

Jana, K.

I. Dey, K. Jana, V. Y. Fedorov, A. D. Koulouklidis, A. Mondal, M. Shaikh, D. Sarkar, A. D. Lad, S. Tzortzakis, A. Couairon, and G. R. Kumar, “Highly efficient broadband terahertz generation from ultrashort laser filamentation in liquids,” Nat. Commun. 8(1), 1184 (2017).
[Crossref] [PubMed]

Jarrahi, M.

N. T. Yardimci, S. Cakmakyapan, S. Hemmati, and M. Jarrahi, “A High-Power Broadband Terahertz Source Enabled by Three-Dimensional Light Confinement in a Plasmonic Nanocavity,” Sci. Rep. 7(1), 4166 (2017).
[Crossref] [PubMed]

Jemal, A.

R. L. Siegel, K. D. Miller, and A. Jemal, “Cancer Statistics, 2015,” CA Cancer J. Clin. 65(1), 5–29 (2015).
[Crossref] [PubMed]

Jiang, L.

C. Zhang, L. Liang, L. Ding, B. Jin, Y. Hou, C. Li, L. Jiang, W. Liu, W. Hu, Y. Lu, L. Kang, W. Xu, J. Chen, and P. Wu, “Label-free measurements on cell apoptosis using a terahertz metamaterial-based biosensor,” Appl. Phys. Lett. 108(24), 241105 (2016).
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C. Zhang, L. Liang, L. Ding, B. Jin, Y. Hou, C. Li, L. Jiang, W. Liu, W. Hu, Y. Lu, L. Kang, W. Xu, J. Chen, and P. Wu, “Label-free measurements on cell apoptosis using a terahertz metamaterial-based biosensor,” Appl. Phys. Lett. 108(24), 241105 (2016).
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Jing, X.

Kaczmarek, A.

A. Kaczmarek, P. Vandenabeele, and D. V. Krysko, “Necroptosis: The Release of Damage-Associated Molecular Patterns and Its Physiological Relevance,” Immunity 38(2), 209–223 (2013).
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Kamal, A.

A. Kamal, S. Faazil, and M. S. Malik, “Apoptosis-inducing agents: A patent review (2010 - 2013),” Expert Opin. Ther. Pat. 24(3), 339–354 (2014).
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Kang, L.

C. Zhang, L. Liang, L. Ding, B. Jin, Y. Hou, C. Li, L. Jiang, W. Liu, W. Hu, Y. Lu, L. Kang, W. Xu, J. Chen, and P. Wu, “Label-free measurements on cell apoptosis using a terahertz metamaterial-based biosensor,” Appl. Phys. Lett. 108(24), 241105 (2016).
[Crossref]

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H. Tao, L. R. Chieffo, M. A. Brenckle, S. M. Siebert, M. Liu, A. C. Strikwerda, K. Fan, D. L. Kaplan, X. Zhang, R. D. Averitt, and F. G. Omenetto, “Metamaterials on Paper as a Sensing Platform,” Adv. Mater. 23(28), 3197–3201 (2011).
[Crossref] [PubMed]

Kats, M. A.

N. Yu, P. Genevet, M. A. Kats, F. Aieta, J. P. Tetienne, F. Capasso, and Z. Gaburro, “Light propagation with phase discontinuities: generalized laws of reflection and refraction,” Science 334(6054), 333–337 (2011).
[Crossref] [PubMed]

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H. Iwasaki, M. Nakamura, N. Komatsubara, M. Okano, M. Nakasako, H. Sato, and S. Watanabe, “Controlled Terahertz Birefringence in Stretched Poly(lactic acid) Films Investigated by Terahertz Time-Domain Spectroscopy and Wide-Angle X-ray Scattering,” J. Phys. Chem. B 121(28), 6951–6957 (2017).
[Crossref] [PubMed]

Koulouklidis, A. D.

I. Dey, K. Jana, V. Y. Fedorov, A. D. Koulouklidis, A. Mondal, M. Shaikh, D. Sarkar, A. D. Lad, S. Tzortzakis, A. Couairon, and G. R. Kumar, “Highly efficient broadband terahertz generation from ultrashort laser filamentation in liquids,” Nat. Commun. 8(1), 1184 (2017).
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Krysko, D. V.

A. Kaczmarek, P. Vandenabeele, and D. V. Krysko, “Necroptosis: The Release of Damage-Associated Molecular Patterns and Its Physiological Relevance,” Immunity 38(2), 209–223 (2013).
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Kumar, G. R.

I. Dey, K. Jana, V. Y. Fedorov, A. D. Koulouklidis, A. Mondal, M. Shaikh, D. Sarkar, A. D. Lad, S. Tzortzakis, A. Couairon, and G. R. Kumar, “Highly efficient broadband terahertz generation from ultrashort laser filamentation in liquids,” Nat. Commun. 8(1), 1184 (2017).
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I. Dey, K. Jana, V. Y. Fedorov, A. D. Koulouklidis, A. Mondal, M. Shaikh, D. Sarkar, A. D. Lad, S. Tzortzakis, A. Couairon, and G. R. Kumar, “Highly efficient broadband terahertz generation from ultrashort laser filamentation in liquids,” Nat. Commun. 8(1), 1184 (2017).
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Law, S.

Lee, M.

W. J. Padilla, M. T. Aronsson, C. Highstrete, M. Lee, A. J. Taylor, and R. D. Averitt, “Electrically resonant terahertz metamaterials: Theoretical and experimental investigations,” Phys. Rev. B 75(4), 041102 (2007).
[Crossref]

H.-T. Chen, J. F. O’Hara, A. J. Taylor, R. D. Averitt, C. Highstrete, M. Lee, and W. J. Padilla, “Complementary planar terahertz metamaterials,” Opt. Express 15(3), 1084–1095 (2007).
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B. Levine and J. Yuan, “Autophagy in cell death: An innocent convict?” J. Clin. Invest. 115(10), 2679–2688 (2005).
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C. Zhang, L. Liang, L. Ding, B. Jin, Y. Hou, C. Li, L. Jiang, W. Liu, W. Hu, Y. Lu, L. Kang, W. Xu, J. Chen, and P. Wu, “Label-free measurements on cell apoptosis using a terahertz metamaterial-based biosensor,” Appl. Phys. Lett. 108(24), 241105 (2016).
[Crossref]

Li, J.

Li, S.

C. Cao, J. Zhang, X. Wen, S. L. Dodson, N. T. Dao, L. M. Wong, S. Wang, S. Li, A. T. Phan, and Q. Xiong, “Metamaterials-Based Label-Free Nanosensor for Conformation and Affinity Biosensing,” ACS Nano 7(9), 7583–7591 (2013).
[Crossref] [PubMed]

Li, Z.

Lian, F.

Liang, E.

Liang, L.

C. Zhang, L. Liang, L. Ding, B. Jin, Y. Hou, C. Li, L. Jiang, W. Liu, W. Hu, Y. Lu, L. Kang, W. Xu, J. Chen, and P. Wu, “Label-free measurements on cell apoptosis using a terahertz metamaterial-based biosensor,” Appl. Phys. Lett. 108(24), 241105 (2016).
[Crossref]

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S.-L. Chen, Y.-C. Chang, C. Zhang, J. G. Ok, T. Ling, M. T. Mihnev, T. B. Norris, and L. J. Guo, “Efficient real-time detection of terahertz pulse radiation based on photoacoustic conversion by carbon nanotube nanocomposite,” Nat. Photonics 8(7), 537–542 (2014).
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H. Tao, L. R. Chieffo, M. A. Brenckle, S. M. Siebert, M. Liu, A. C. Strikwerda, K. Fan, D. L. Kaplan, X. Zhang, R. D. Averitt, and F. G. Omenetto, “Metamaterials on Paper as a Sensing Platform,” Adv. Mater. 23(28), 3197–3201 (2011).
[Crossref] [PubMed]

Liu, Q.

Liu, W.

C. Zhang, L. Liang, L. Ding, B. Jin, Y. Hou, C. Li, L. Jiang, W. Liu, W. Hu, Y. Lu, L. Kang, W. Xu, J. Chen, and P. Wu, “Label-free measurements on cell apoptosis using a terahertz metamaterial-based biosensor,” Appl. Phys. Lett. 108(24), 241105 (2016).
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Lu, Y.

C. Zhang, L. Liang, L. Ding, B. Jin, Y. Hou, C. Li, L. Jiang, W. Liu, W. Hu, Y. Lu, L. Kang, W. Xu, J. Chen, and P. Wu, “Label-free measurements on cell apoptosis using a terahertz metamaterial-based biosensor,” Appl. Phys. Lett. 108(24), 241105 (2016).
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K. Batrakov and S. Maksimenko, “Graphene layered systems as a terahertz source with tuned frequency,” Phys. Rev. B 95(20), 205408 (2017).
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A. Kamal, S. Faazil, and M. S. Malik, “Apoptosis-inducing agents: A patent review (2010 - 2013),” Expert Opin. Ther. Pat. 24(3), 339–354 (2014).
[Crossref] [PubMed]

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S.-L. Chen, Y.-C. Chang, C. Zhang, J. G. Ok, T. Ling, M. T. Mihnev, T. B. Norris, and L. J. Guo, “Efficient real-time detection of terahertz pulse radiation based on photoacoustic conversion by carbon nanotube nanocomposite,” Nat. Photonics 8(7), 537–542 (2014).
[Crossref]

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R. L. Siegel, K. D. Miller, and A. Jemal, “Cancer Statistics, 2015,” CA Cancer J. Clin. 65(1), 5–29 (2015).
[Crossref] [PubMed]

Mittleman, D.

Mondal, A.

I. Dey, K. Jana, V. Y. Fedorov, A. D. Koulouklidis, A. Mondal, M. Shaikh, D. Sarkar, A. D. Lad, S. Tzortzakis, A. Couairon, and G. R. Kumar, “Highly efficient broadband terahertz generation from ultrashort laser filamentation in liquids,” Nat. Commun. 8(1), 1184 (2017).
[Crossref] [PubMed]

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H. Iwasaki, M. Nakamura, N. Komatsubara, M. Okano, M. Nakasako, H. Sato, and S. Watanabe, “Controlled Terahertz Birefringence in Stretched Poly(lactic acid) Films Investigated by Terahertz Time-Domain Spectroscopy and Wide-Angle X-ray Scattering,” J. Phys. Chem. B 121(28), 6951–6957 (2017).
[Crossref] [PubMed]

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H. Iwasaki, M. Nakamura, N. Komatsubara, M. Okano, M. Nakasako, H. Sato, and S. Watanabe, “Controlled Terahertz Birefringence in Stretched Poly(lactic acid) Films Investigated by Terahertz Time-Domain Spectroscopy and Wide-Angle X-ray Scattering,” J. Phys. Chem. B 121(28), 6951–6957 (2017).
[Crossref] [PubMed]

Nickel, D.

Norris, T. B.

S.-L. Chen, Y.-C. Chang, C. Zhang, J. G. Ok, T. Ling, M. T. Mihnev, T. B. Norris, and L. J. Guo, “Efficient real-time detection of terahertz pulse radiation based on photoacoustic conversion by carbon nanotube nanocomposite,” Nat. Photonics 8(7), 537–542 (2014).
[Crossref]

O’Hara, J. F.

Ok, J. G.

S.-L. Chen, Y.-C. Chang, C. Zhang, J. G. Ok, T. Ling, M. T. Mihnev, T. B. Norris, and L. J. Guo, “Efficient real-time detection of terahertz pulse radiation based on photoacoustic conversion by carbon nanotube nanocomposite,” Nat. Photonics 8(7), 537–542 (2014).
[Crossref]

Okano, M.

H. Iwasaki, M. Nakamura, N. Komatsubara, M. Okano, M. Nakasako, H. Sato, and S. Watanabe, “Controlled Terahertz Birefringence in Stretched Poly(lactic acid) Films Investigated by Terahertz Time-Domain Spectroscopy and Wide-Angle X-ray Scattering,” J. Phys. Chem. B 121(28), 6951–6957 (2017).
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H. Tao, L. R. Chieffo, M. A. Brenckle, S. M. Siebert, M. Liu, A. C. Strikwerda, K. Fan, D. L. Kaplan, X. Zhang, R. D. Averitt, and F. G. Omenetto, “Metamaterials on Paper as a Sensing Platform,” Adv. Mater. 23(28), 3197–3201 (2011).
[Crossref] [PubMed]

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H.-T. Chen, J. F. O’Hara, A. J. Taylor, R. D. Averitt, C. Highstrete, M. Lee, and W. J. Padilla, “Complementary planar terahertz metamaterials,” Opt. Express 15(3), 1084–1095 (2007).
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W. J. Padilla, M. T. Aronsson, C. Highstrete, M. Lee, A. J. Taylor, and R. D. Averitt, “Electrically resonant terahertz metamaterials: Theoretical and experimental investigations,” Phys. Rev. B 75(4), 041102 (2007).
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Palacios, J.

Phan, A. T.

C. Cao, J. Zhang, X. Wen, S. L. Dodson, N. T. Dao, L. M. Wong, S. Wang, S. Li, A. T. Phan, and Q. Xiong, “Metamaterials-Based Label-Free Nanosensor for Conformation and Affinity Biosensing,” ACS Nano 7(9), 7583–7591 (2013).
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Redo-Sanchez, A.

Sarkar, D.

I. Dey, K. Jana, V. Y. Fedorov, A. D. Koulouklidis, A. Mondal, M. Shaikh, D. Sarkar, A. D. Lad, S. Tzortzakis, A. Couairon, and G. R. Kumar, “Highly efficient broadband terahertz generation from ultrashort laser filamentation in liquids,” Nat. Commun. 8(1), 1184 (2017).
[Crossref] [PubMed]

Sato, H.

H. Iwasaki, M. Nakamura, N. Komatsubara, M. Okano, M. Nakasako, H. Sato, and S. Watanabe, “Controlled Terahertz Birefringence in Stretched Poly(lactic acid) Films Investigated by Terahertz Time-Domain Spectroscopy and Wide-Angle X-ray Scattering,” J. Phys. Chem. B 121(28), 6951–6957 (2017).
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R. A. Shelby, D. R. Smith, and S. Schultz, “Experimental Verification of a Negative Index of Refraction,” Science 292(5514), 77–79 (2001).
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Shaikh, M.

I. Dey, K. Jana, V. Y. Fedorov, A. D. Koulouklidis, A. Mondal, M. Shaikh, D. Sarkar, A. D. Lad, S. Tzortzakis, A. Couairon, and G. R. Kumar, “Highly efficient broadband terahertz generation from ultrashort laser filamentation in liquids,” Nat. Commun. 8(1), 1184 (2017).
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R. A. Shelby, D. R. Smith, and S. Schultz, “Experimental Verification of a Negative Index of Refraction,” Science 292(5514), 77–79 (2001).
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H. Tao, L. R. Chieffo, M. A. Brenckle, S. M. Siebert, M. Liu, A. C. Strikwerda, K. Fan, D. L. Kaplan, X. Zhang, R. D. Averitt, and F. G. Omenetto, “Metamaterials on Paper as a Sensing Platform,” Adv. Mater. 23(28), 3197–3201 (2011).
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R. L. Siegel, K. D. Miller, and A. Jemal, “Cancer Statistics, 2015,” CA Cancer J. Clin. 65(1), 5–29 (2015).
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L. Cong, S. Tan, R. Yahiaoui, F. Yan, W. Zhang, and R. Singh, “Experimental demonstration of ultrasensitive sensing with terahertz metamaterial absorbers: A comparison with the metasurfaces,” Appl. Phys. Lett. 106(3), 031107 (2015).
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Smith, D. R.

R. A. Shelby, D. R. Smith, and S. Schultz, “Experimental Verification of a Negative Index of Refraction,” Science 292(5514), 77–79 (2001).
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Strikwerda, A. C.

H. Tao, L. R. Chieffo, M. A. Brenckle, S. M. Siebert, M. Liu, A. C. Strikwerda, K. Fan, D. L. Kaplan, X. Zhang, R. D. Averitt, and F. G. Omenetto, “Metamaterials on Paper as a Sensing Platform,” Adv. Mater. 23(28), 3197–3201 (2011).
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Tan, S.

L. Cong, S. Tan, R. Yahiaoui, F. Yan, W. Zhang, and R. Singh, “Experimental demonstration of ultrasensitive sensing with terahertz metamaterial absorbers: A comparison with the metasurfaces,” Appl. Phys. Lett. 106(3), 031107 (2015).
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H. Tao, L. R. Chieffo, M. A. Brenckle, S. M. Siebert, M. Liu, A. C. Strikwerda, K. Fan, D. L. Kaplan, X. Zhang, R. D. Averitt, and F. G. Omenetto, “Metamaterials on Paper as a Sensing Platform,” Adv. Mater. 23(28), 3197–3201 (2011).
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H.-T. Chen, J. F. O’Hara, A. J. Taylor, R. D. Averitt, C. Highstrete, M. Lee, and W. J. Padilla, “Complementary planar terahertz metamaterials,” Opt. Express 15(3), 1084–1095 (2007).
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W. J. Padilla, M. T. Aronsson, C. Highstrete, M. Lee, A. J. Taylor, and R. D. Averitt, “Electrically resonant terahertz metamaterials: Theoretical and experimental investigations,” Phys. Rev. B 75(4), 041102 (2007).
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Tejada, J.

Tetienne, J. P.

N. Yu, P. Genevet, M. A. Kats, F. Aieta, J. P. Tetienne, F. Capasso, and Z. Gaburro, “Light propagation with phase discontinuities: generalized laws of reflection and refraction,” Science 334(6054), 333–337 (2011).
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Tian, Y.

Tzortzakis, S.

I. Dey, K. Jana, V. Y. Fedorov, A. D. Koulouklidis, A. Mondal, M. Shaikh, D. Sarkar, A. D. Lad, S. Tzortzakis, A. Couairon, and G. R. Kumar, “Highly efficient broadband terahertz generation from ultrashort laser filamentation in liquids,” Nat. Commun. 8(1), 1184 (2017).
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Vandenabeele, P.

A. Kaczmarek, P. Vandenabeele, and D. V. Krysko, “Necroptosis: The Release of Damage-Associated Molecular Patterns and Its Physiological Relevance,” Immunity 38(2), 209–223 (2013).
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Wang, J.

Wang, S.

C. Cao, J. Zhang, X. Wen, S. L. Dodson, N. T. Dao, L. M. Wong, S. Wang, S. Li, A. T. Phan, and Q. Xiong, “Metamaterials-Based Label-Free Nanosensor for Conformation and Affinity Biosensing,” ACS Nano 7(9), 7583–7591 (2013).
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H. Iwasaki, M. Nakamura, N. Komatsubara, M. Okano, M. Nakasako, H. Sato, and S. Watanabe, “Controlled Terahertz Birefringence in Stretched Poly(lactic acid) Films Investigated by Terahertz Time-Domain Spectroscopy and Wide-Angle X-ray Scattering,” J. Phys. Chem. B 121(28), 6951–6957 (2017).
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Wen, X.

C. Cao, J. Zhang, X. Wen, S. L. Dodson, N. T. Dao, L. M. Wong, S. Wang, S. Li, A. T. Phan, and Q. Xiong, “Metamaterials-Based Label-Free Nanosensor for Conformation and Affinity Biosensing,” ACS Nano 7(9), 7583–7591 (2013).
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C. Cao, J. Zhang, X. Wen, S. L. Dodson, N. T. Dao, L. M. Wong, S. Wang, S. Li, A. T. Phan, and Q. Xiong, “Metamaterials-Based Label-Free Nanosensor for Conformation and Affinity Biosensing,” ACS Nano 7(9), 7583–7591 (2013).
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Wu, P.

C. Zhang, L. Liang, L. Ding, B. Jin, Y. Hou, C. Li, L. Jiang, W. Liu, W. Hu, Y. Lu, L. Kang, W. Xu, J. Chen, and P. Wu, “Label-free measurements on cell apoptosis using a terahertz metamaterial-based biosensor,” Appl. Phys. Lett. 108(24), 241105 (2016).
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Xiong, Q.

C. Cao, J. Zhang, X. Wen, S. L. Dodson, N. T. Dao, L. M. Wong, S. Wang, S. Li, A. T. Phan, and Q. Xiong, “Metamaterials-Based Label-Free Nanosensor for Conformation and Affinity Biosensing,” ACS Nano 7(9), 7583–7591 (2013).
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C. Zhang, L. Liang, L. Ding, B. Jin, Y. Hou, C. Li, L. Jiang, W. Liu, W. Hu, Y. Lu, L. Kang, W. Xu, J. Chen, and P. Wu, “Label-free measurements on cell apoptosis using a terahertz metamaterial-based biosensor,” Appl. Phys. Lett. 108(24), 241105 (2016).
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Yahiaoui, R.

L. Cong, S. Tan, R. Yahiaoui, F. Yan, W. Zhang, and R. Singh, “Experimental demonstration of ultrasensitive sensing with terahertz metamaterial absorbers: A comparison with the metasurfaces,” Appl. Phys. Lett. 106(3), 031107 (2015).
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L. Cong, S. Tan, R. Yahiaoui, F. Yan, W. Zhang, and R. Singh, “Experimental demonstration of ultrasensitive sensing with terahertz metamaterial absorbers: A comparison with the metasurfaces,” Appl. Phys. Lett. 106(3), 031107 (2015).
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N. T. Yardimci, S. Cakmakyapan, S. Hemmati, and M. Jarrahi, “A High-Power Broadband Terahertz Source Enabled by Three-Dimensional Light Confinement in a Plasmonic Nanocavity,” Sci. Rep. 7(1), 4166 (2017).
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Yuan, J.

B. Levine and J. Yuan, “Autophagy in cell death: An innocent convict?” J. Clin. Invest. 115(10), 2679–2688 (2005).
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C. Zhang, L. Liang, L. Ding, B. Jin, Y. Hou, C. Li, L. Jiang, W. Liu, W. Hu, Y. Lu, L. Kang, W. Xu, J. Chen, and P. Wu, “Label-free measurements on cell apoptosis using a terahertz metamaterial-based biosensor,” Appl. Phys. Lett. 108(24), 241105 (2016).
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S.-L. Chen, Y.-C. Chang, C. Zhang, J. G. Ok, T. Ling, M. T. Mihnev, T. B. Norris, and L. J. Guo, “Efficient real-time detection of terahertz pulse radiation based on photoacoustic conversion by carbon nanotube nanocomposite,” Nat. Photonics 8(7), 537–542 (2014).
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C. Cao, J. Zhang, X. Wen, S. L. Dodson, N. T. Dao, L. M. Wong, S. Wang, S. Li, A. T. Phan, and Q. Xiong, “Metamaterials-Based Label-Free Nanosensor for Conformation and Affinity Biosensing,” ACS Nano 7(9), 7583–7591 (2013).
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H. Tao, L. R. Chieffo, M. A. Brenckle, S. M. Siebert, M. Liu, A. C. Strikwerda, K. Fan, D. L. Kaplan, X. Zhang, R. D. Averitt, and F. G. Omenetto, “Metamaterials on Paper as a Sensing Platform,” Adv. Mater. 23(28), 3197–3201 (2011).
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Zhao, J. H.

Zhao, P.

Zhu, L. G.

Zolliker, P.

Zotova, I. B.

ACS Nano (1)

C. Cao, J. Zhang, X. Wen, S. L. Dodson, N. T. Dao, L. M. Wong, S. Wang, S. Li, A. T. Phan, and Q. Xiong, “Metamaterials-Based Label-Free Nanosensor for Conformation and Affinity Biosensing,” ACS Nano 7(9), 7583–7591 (2013).
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Adv. Mater. (1)

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Figures (5)

Fig. 1
Fig. 1 (a) The schematic of MMs-based transmission-type biosensor comprised of periodic SRRs/dielectric unit cells, the incident THz waves propagated through MMs from bottom dielectric to top metal layer. (b) According top view and side view of the unit cell were shown, respectively. The structural parameters: a = 36 μm, l = 4 μm, d = 3.5 μm, s = 4 μm and h = 10 μm. (c) The micrograph of fabricated MMs sample, the 1cm×1cm biosensor was given in inset. (d) A color-enhanced micrograph of MMs coated by HSC3 cells.
Fig. 2
Fig. 2 (a) The simulate and experimentally measured transmission spectrum of the designed SRRs structure. Corresponding surface current density (the orientation and colour of arrows indicate the direction and relative magnitude of the surface current density, respectively) and electric field (the color shows the relative local electric field amplitude) at lower frequency 0.85 THz (b) and higher frequency 3.6 THz (c), respectively.
Fig. 3
Fig. 3 (a) The simulate transmission spectrum of the designed SRRs structure under different occupying ratio (OR) of analyte disk to unit cell of structure. (b) The dependence of resonant frequency shift Δf on OR values. (c) The simulate transmission of the designed SRRs structure under different analyte dielectric constants. (d) The dependence of resonant frequency shift Δf on analyte dielectric constants, the sensitivity can be obtained from the linear relationship of the two parameters.
Fig. 4
Fig. 4 (a) The measured transmission of the designed MMs-based biosensors under different cell concentrations, 1×105cell/ml, 2×105cell/ml and 3×105cell/ml, respectively. (b) The dependence of resonant frequency shift Δf on cell concentration extracted from (a).
Fig. 5
Fig. 5 (a) The measured transmission spectrum of biosensors with cancer cells under the effect of 1μM, 8 μM and 15 μM cisplatin for 72 hours, respectively. (b) The measured transmission spectrum of biosensors with cancer cells under 15 μM cisplatin effect for 24h, 48 h and 72 h, respectively. (c) The extracted frequency shift Δf and measured apoptosis CCK-8 method under the effect of cisplatin with different drug concentrations. (d) The extracted frequency shift Δf and measured apoptosis CCK-8 method under the effect of different durations of drug action.

Equations (1)

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Δ ω ω 0 = v 0 ( Δ ε | E ¯ 0 | 2 + Δ μ | H ¯ 0 | 2 ) d v v 0 ( ε | E ¯ 0 | 2 + μ | H ¯ 0 | 2 ) d v v 0 ( Δ ε | E ¯ 0 | 2 ) d v 2 v 0 ( ε | E ¯ 0 | 2 ) d v

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