Fluorescence for biological logic gates
Eran A. Barnoy
Faculty of Engineering and the Institute of Nanotechnology and Advanced Materials, Bar Ilan University, Ramat Gan, Israel
Search for more papers by this authorRachela Popovtzer
Faculty of Engineering and the Institute of Nanotechnology and Advanced Materials, Bar Ilan University, Ramat Gan, Israel
Search for more papers by this authorCorresponding Author
Dror Fixler
Faculty of Engineering and the Institute of Nanotechnology and Advanced Materials, Bar Ilan University, Ramat Gan, Israel
Correspondence
Dror Fixler, Faculty of Engineering and the Institute of Nanotechnology and Advanced Materials, Bar Ilan University, Ramat Gan 5290002, Israel.
Email: [email protected]
Search for more papers by this authorEran A. Barnoy
Faculty of Engineering and the Institute of Nanotechnology and Advanced Materials, Bar Ilan University, Ramat Gan, Israel
Search for more papers by this authorRachela Popovtzer
Faculty of Engineering and the Institute of Nanotechnology and Advanced Materials, Bar Ilan University, Ramat Gan, Israel
Search for more papers by this authorCorresponding Author
Dror Fixler
Faculty of Engineering and the Institute of Nanotechnology and Advanced Materials, Bar Ilan University, Ramat Gan, Israel
Correspondence
Dror Fixler, Faculty of Engineering and the Institute of Nanotechnology and Advanced Materials, Bar Ilan University, Ramat Gan 5290002, Israel.
Email: [email protected]
Search for more papers by this authorFunding information: Israel Science Foundation, Grant/Award Number: 1195/18; Israeli Ministry of Science, Technology, and Space, Grant/Award Number: 3-13334
Abstract
Biological logic gates are smart probes able to respond to biological conditions in behaviors similar to computer logic gates, and they pose a promising challenge for modern medicine. Researchers are creating many kinds of smart nanostructures that can respond to various biological parameters such as pH, ion presence, and enzyme activity. Each of these conditions alone might be interesting in a biological sense, but their interactions are what define specific disease conditions. Researchers over the past few decades have developed a plethora of stimuli-responsive nanodevices, from activatable fluorescent probes to DNA origami nanomachines, many explicitly defining logic operations. Whereas many smart configurations have been explored, in this review we focus on logic operations actuated through fluorescent signals. We discuss the applicability of fluorescence as a means of logic gate implementation, and consider the use of both fluorescence intensity as well as fluorescence lifetime.
CONFLICT OF INTEREST
The authors declare no financial or commercial conflict of interest.
REFERENCES
- 1M. Jiao, P. Zhang, J. Meng, Y. Li, C. Liu, X. Luo, M. Gao, Biomater. Sci. 2018, 6, 726.
- 2I. L. Sokolov, V. R. Cherkasov, A. A. Tregubov, S. R. Buiucli, M. P. Nikitin, Biochim. Biophys. Acta - Gen. Subj. 2017, 1861, 1530.
- 3Y. Lu, A. A. Aimetti, R. Langer, Z. Gu, Nat. Rev. Mater. 2017, 2, 16075.
- 4N. Hanafy, S. Leporatti, M. El-Kemary, Appl. Sci. 2019, 9, 825.
- 5J. Liao, Y. Jia, Y. Wu, K. Shi, D. Yang, P. Li, Z. Qian, WIREs Nanomed. Nanobiotechnol. 2020, 12, e1581.
- 6M. Zhang, X. Chen, C. Li, X. Shen, J. Control. Release 2020, 319, 46.
- 7T. Ma, P. Zhang, Y. Hou, H. Ning, Z. Wang, J. Huang, M. Gao, Adv. Healthc. Mater. 2018, 7, 1800391.
- 8V. Balzani, A. Credi, M. Venturi, ChemPhysChem 2003, 4, 49.
- 9A. C. Evans, N. N. Thadani, J. Suh, J. Control. Release 2016, 240, 387.
- 10E. Katz, J. Wang, J. Halamek, L. Halamkova, in Label-Free Biosensing, Vol. 16 (Eds: M. Schöning, A. Poghossian), Springer, Cham, Switzerland 2017, p. 345.
10.1007/5346_2017_4 Google Scholar
- 11J. Du, L. A. Lane, S. Nie, J. Control. Release 2015, 219, 205.
- 12J. Andréasson, U. Pischel, Chem. Soc. Rev. 2015, 44, 1053.
- 13D. Rosenblum, N. Joshi, W. Tao, J. M. Karp, D. Peer, Nat. Commun. 2018, 9, 1410.
- 14T. Miyamoto, S. Razavi, R. DeRose, T. Inoue, ACS Synth. Biol. 2013, 2, 72.
- 15E. Fleige, M. A. Quadir, R. Haag, Adv. Drug Deliv. Rev. 2012, 64, 866.
- 16R. Cheng, F. Meng, C. Deng, H. Klok, Z. Zhong, Biomaterials 2013, 34, 3647.
- 17B. Wilson, Z. Wu, Biomaterials 2016, 85, 152.
- 18R. Oliveira-Silva, M. Sousa-Jerónimo, D. Botequim, N. J. O. Silva, P. M. R. Paulo, D. M. F. Prazeres, Trends Biochem. Sci. 2020, 20, 30088.
- 19H. Ijäs, S. Nummelin, B. Shen, M. A. Kostiainen, V. Linko, Int. J. Mol. Sci. 2018, 19, 2114.
- 20C. R. Drake, D. C. Miller, E. F. Jones, Curr. Org. Synth. 2011, 8, 498.
- 21H. Kobayashi, P. L. Choyke, Acc. Chem. Res. 2011, 44, 83.
- 22Y. Wang, Y. Zhang, J. Wang, X. J. Liang, Adv. Drug Deliv. Rev. 2019, 143, 161.
- 23H. Ehtesabi, Z. Hallaji, S. Najafi Nobar, Z. Bagheri, Microchim. Acta 2020, 187, 1.
- 24S. Chen, L. Rong, Q. Lei, P.-X. Cao, S.-Y. Qin, D.-W. Zheng, H.-Z. Jia, J.-Y. Zhu, S.-X. Cheng, R.-X. Zhuo, X.-Z. Zhang, Biomaterials 2016, 77, 149.
- 25W. J. Niu, D. Shan, R. H. Zhu, S. Y. Deng, S. Cosnier, X. J. Zhang, Carbon N. Y. 2016, 96, 1034.
- 26E. Barnoy, M. Motiei, C. Tzror, S. Rahimipour, R. Popovtzer, D. Fixler, ACS Appl. Nano Mater. 2019, 2(10), 6527.
- 27T. Cui, J. J. Liang, H. Chen, D. D. Geng, L. Jiao, J. Y. Yang, H. Qian, C. Zhang, Y. Ding, ACS Appl. Mater. Interfaces 2017, 9, 8569.
- 28P. Zhang, D. Gao, K. An, Q. Shen, C. Wang, Y. Zhang, X. Pan, X. Chen, Y. Lyv, C. Cui, T. Liang, X. Duan, J. Liu, T. Yang, X. Hu, J. J. Zhu, F. Xu, W. Tan, Nat. Chem. 2020, 12, 381.
- 29K. K. Karukstis, E. H. Z. Thompson, J. A. Whiles, R. J. Rosenfeld, Biophys. Chem. 1998, 73, 249.
- 30J. A. Thomas, Chem. Soc. Rev. 2015, 44, 4494.
- 31M. P. Nikitin, V. O. Shipunova, S. M. Deyev, P. I. Nikitin, Nat. Nanotechnol. 2014, 9, 716.
- 32J.-H. Zhu, M.-M. Li, S.-P. Liu, Z.-F. Liu, Y.-F. Li, X.-L. Hu, Sens. Actuators B 2015, 219, 261.
- 33H. Bui, C. W. Brown, S. Buckhout-White, S. A. Díaz, M. H. Stewart, K. Susumu, E. Oh, M. G. Ancona, E. R. Goldman, I. L. Medintz, Small 2019, 15, 1805384.
- 34E. A. Barnoy, R. Popovtzer, D. Fixler, J. Biophotonics 2018, 11, e201700084.
- 35P. Loison, N. A. Hosny, P. Gervais, D. Champion, M. K. Kuimova, J.-M. Perrier-Cornet, Biochim. Biophys. Acta - Biomembr. 1828, 2013, 2436.
- 36M. Tripathy, U. Subuddhi, S. Patel, Dye. Pigment. 2020, 174, 108054.
- 37J. R. Lakowicz, Anal. Biochem. 2005, 337, 171.
- 38E. A. Barnoy, D. Fixler, R. Popovtzer, T. Nayhoz, K. Ray, Nano Res. 2015, 8, 3912.
- 39T. Nayhoz, E. A. Barnoy, D. Fixler, Materials (Basel). 2016, 9, 926.
- 40P. G. Mahajan, G. B. Kolekar, S. R. Patil, Luminescence 2017, 32, 845.
- 41K. Suhling, L. M. Hirvonen, J. A. Levitt, P.-H. Chung, C. Tregidgo, A. Le Marois, D. A. Rusakov, K. Zheng, S. Ameer-Beg, S. Poland, S. Coelho, R. Henderson, N. Krstajic, Med. Photonics 2015, 27, 3.
- 42Z. Gu, A. A. Aimetti, Q. Wang, T. T. Dang, Y. Zhang, O. Veiseh, H. Cheng, R. S. Langer, D. G. Anderson, ACS Nano 2013, 7, 4194.
- 43T. Tian, Y. Zhong, C. Deng, H. Wang, Y. He, Y. Ge, G. Song, Talanta 2017, 162, 135.
- 44Y. Yuan, J. Jiang, S. Liu, J. Yang, H. zhang, J. Yan, X. Hu, Sens. Actuators B 2017, 242, 545.
- 45Y.-S. He, C.-G. Pan, H.-X. Cao, M.-Z. Yue, L. Wang, G.-X. Liang, Sens. Actuators B 2018, 265, 371.
- 46M. Motiei, T. Dreifuss, O. Betzer, H. Panet, A. Popovtzer, J. Santana, G. Abourbeh, E. Mishani, R. Popovtzer, ACS Nano 2016, 10, 3469.
- 47X. Zhao, C. X. Yang, L. G. Chen, X. P. Yan, Nat. Commun. 2017, 8, 14998.
- 48D. B. Pacardo, F. S. Ligler, Z. Gu, Nanoscale 2015, 7, 3381.
- 49T. Wang, D. Wang, J. Liu, B. Feng, F. Zhou, H. Zhang, L. Zhou, Q. Yin, Z. Zhang, Z. Cao, H. Yu, Y. Li, Nano Lett. 2017, 17, 5429.
- 50S. Ruan, X. Cao, X. Cun, G. Hu, Y. Zhou, Y. Zhang, L. Lu, Q. He, H. Gao, Biomaterials 2015, 60, 100.
- 51H.-J. Li, J.-Z. Du, X.-J. Du, C.-F. Xu, C.-Y. Sun, H.-X. Wang, Z.-T. Cao, X.-Z. Yang, Y.-H. Zhu, S. Nie, J. Wang, Proc. Natl. Acad. Sci. USA 2016, 113, 4164.
- 52S. Chen, Q. Lei, S.-Y. Li, S.-Y. Qin, H.-Z. Jia, Y.-J. Cheng, X.-Z. Zhang, Biomaterials 2016, 92, 25.
- 53G. Chen, Y. Wang, R. Xie, S. Gong, J. Control. Release 2017, 259, 105.
- 54C. Yan, Z. Guo, Y. Liu, P. Shi, H. Tian, W. H. Zhu, Chem. Sci. 2018, 9, 6176.
- 55H. Han, D. Valdepérez, Q. Jin, B. Yang, Z. Li, Y. Wu, B. Pelaz, W. J. Parak, J. Ji, ACS Nano 2017, 11, 1281.
- 56D. Xiao, H. Z. Jia, J. Zhang, C. W. Liu, R. X. Zhuo, X. Z. Zhang, Small 2014, 10, 591.
- 57L. Han, C. Tang, C. Yin, ACS Appl. Mater. Interfaces 2016, 8, 23498.
- 58Z. Liu, X. Chen, X. Zhang, J. J. Gooding, Y. Zhou, Adv. Healthc. Mater. 2016, 5, 1401.
- 59A. Unciti-Broceta, Nat. Chem. 2015, 7, 538.
- 60A. Miyawaki, J. Llopis, R. Heim, J. M. McCaffery, J. a Adams, M. Ikura, R. Y. Tsien, Nature 1997, 388, 882.
- 61S. Uchiyama, N. Kawai, A. P. De Silva, K. Iwai, J. Am. Chem. Soc. 2004, 126, 3032.
- 62L. Li, L. Shi, J. Jia, Y. Jiao, Y. Gao, Y. Liu, C. Dong, S. Shuang, Spectrochim. Acta - Part A Mol. Biomol. Spectrosc. 2020, 227, 117716.
- 63Y. Amir, E. Ben-Ishay, D. Levner, S. Ittah, A. Abu-Horowitz, I. Bachelet, Nat. Nanotechnol. 2014, 9, 353.
- 64G. Hu, X. Chun, Y. Wang, Q. He, H. Gao, Oncotarget 2015, 6, 41258.
- 65N. Omersa, S. Aden, M. Kisovec, M. Podobnik, G. Anderluh, ACS Synth. Biol. 2020, 9, 316.
- 66A. P. de Silva, H. Q. N. Gunaratne, C. P. McCoy, Nature 1993, 364, 42.
- 67X. Tian, Z. Dong, J. Hou, R. Wang, J. Ma, JOL 2014, 145, 459.
- 68A. Podder, M. Won, S. Kim, P. Verwilst, M. Maiti, Z. Yang, J. Qu, S. Bhuniya, J. S. Kim, Sens. Actuators B 2018, 268, 195.
- 69C.-B. Bai, R. Qiao, J.-X. Liao, W.-Z. Xiong, J. Zhang, S.-S. Chen, S. Yang, Spectrochim. Acta - Part A Mol. Biomol. Spectrosc. 2018, 202, 252.
- 70Q. Zhai, H. Xing, D. Fan, X. Zhang, J. Li, E. Wang, Sens. Actuators B 2018, 273, 1827.
- 71W.-S. Zou, Q.-C. Zhao, W.-L. Kong, X.-F. Wang, X.-M. Chen, J. Zhang, Y.-Q. Wang, Chem. Eng. J. 2018, 337, 471.
- 72S. Liao, X. Li, H. Yang, X. Chen, Talanta 2019, 194, 554.
- 73P. Ghorai, S. Banerjee, D. Nag, S. K. Mukhopadhyay, A. Saha, JOL 2019, 205, 197.
- 74L. Wu, J. E. Gardiner, L. K. Kumawat, H. H. Han, R. Guo, X. Li, X. P. He, R. B. P. Elmes, A. C. Sedgwick, S. D. Bull, T. D. James, RSC Adv. 2019, 9, 26425.
- 75A. I. Said, N. I. Georgiev, V. B. Bojinov, Spectrochim. Acta - Part A Mol. Biomol. Spectrosc. 2019, 223, 117304.
- 76L. Zhang, J. Qin, Q. Yang, S. Wei, R. Yang, J. Photochem. Photobiol. A Chem. 2019, 382, 111918.
- 77Y. Fang, L. Zhou, J. Zhao, Y. Zhang, M. Yang, C. Yi, Carbon N. Y. 2020, 166, 265.
- 78F. Pu, J. Ren, X. Qu, ACS Appl. Mater. Interfaces 2014, 6, 9557.
- 79M. Prost, J. Hasserodt, Chem. Commun. (Camb.) 2014, 50, 14896.
- 80S. Angelos, Y. Yang, N. M. Khashab, J. F. Stoddart, J. I. Zink, Am. Chem. Soc. 2009, 131, 11344.
- 81P. Remón, R. Ferreira, J.-M. Montenegro, R. Suau, E. Pérez-Inestrosa, U. Pischel, ChemPhysChem 2009, 10, 2004.
- 82S. M. Douglas, I. Bachelet, G. M. Church, Science (80-.). 2012, 335, 831.
- 83W. Chang, W. Liu, H. Shen, S. Chen, P. Liao, Y. Liu, Anal. Chim. Acta 2020, 1112, 46.
- 84T. Chen, X. Fu, Q. Zhang, D. Mao, Y. Song, C. Feng, X. Zhu, Chem. Commun. 2020. https://doi.org/10.1039/d0cc00564a.
- 85Q. Li, Y. He, J. Chang, L. Wang, H. Chen, Y. W. Tan, H. Wang, Z. Shao, J. Am. Chem. Soc. 2013, 135, 14924.
- 86G. Ferri, L. Nucara, T. Biver, A. Battisti, G. Signore, R. Bizzarri, Biophys. Chem. 2016, 208, 17.
- 87P. Pramanik, S. K. Das, M. Halder, J. Phys. Chem. C 2020, 124, 4791.
- 88X. Chen, A. H. Soeriyadi, X. Lu, S. M. Sagnella, M. Kavallaris, J. J. Gooding, Adv. Funct. Mater. 2014, 24, 6999.
- 89A. D. Johnson, K. A. Paterson, J. C. Spiteri, S. A. Denisov, G. Jonusauskas, A. Tron, N. D. McClenaghan, D. C. Magri, New J. Chem. 2016, 40, 9917.
- 90E. A. Barnoy, R. Popovtzer, D. Fixler, Progress in Biomedical Optics and Imaging - Proceedings of SPIE, Vol. no. 10506, SPIE, 2018.
- 91J. C. Spiteri, A. D. Johnson, S. A. Denisov, G. Jonusauskas, N. D. McClenaghan, D. C. Magri, Dyes Pigments 2018, 157, 278.
- 92S. Sahu, T. B. Sil, M. Das, G. Krishnamoorthy, Analyst 2015, 140, 6114.
- 93B. Naskar, R. Modak, Y. Sikdar, D. K. Maiti, A. Banik, T. K. Dangar, S. Mukhopadhyay, D. Mandal, S. Goswami, J. Photochem. Photobiol. A Chem. 2016, 321, 99.
- 94S. Gharami, D. Sarkar, P. Ghosh, S. Acharyya, K. Aich, N. Murmu, T. K. Mondal, Sens. Actuators B 2017, 253, 317.
- 95M. Ghosh, S. Mandal, S. Ta, D. Das, Sens. Actuators B 2017, 249, 339.
- 96Y. Gao, H. Zhang, S. Shuang, H. Han, C. Dong, Anal. Methods 2019, 11, 2650.
- 97T. Daniel Thangadurai, I. Nithya, A. Rakkiyanasamy, Spectrochim. Acta - Part A Mol. Biomol. Spectrosc. 2019, 211, 132.
- 98B. Wang, B. Yan, Talanta 2020, 208, 120438.
- 99M. Eghtedari, A. V. Liopo, J. A. Copland, A. A. Oraevsky, M. Motamedi, Nano Lett. 2009, 9, 287.
- 100M. A. El-Sayed, Acc. Chem. Res. 2001, 34, 257.
- 101P. K. Jain, K. S. Lee, I. H. El-Sayed, M. A. El-Sayed, J. Phys. Chem. B 2006, 110, 7238.
- 102E. Blanco, H. Shen, M. Ferrari, Nat. Biotechnol. 2015, 33, 941.
- 103E. Haimov, H. Weitman, S. Polani, H. Schori, D. Zitoun, O. Shefi, ACS Appl. Mater. Interfaces 2018, 10, 2319.
- 104J. A. Copland, M. Eghtedari, V. L. Popov, N. Kotov, N. Mamedova, M. Motamedi, A. A. Oraevsky, Mol. Imaging Biol. 2004, 6, 341.
- 105X. Qian, X.-H. Peng, D. O. Ansari, Q. Yin-Goen, G. Z. Chen, D. M. Shin, L. Yang, A. N. Young, M. D. Wang, S. Nie, Nat. Biotechnol. 2008, 26, 83.
- 106R. Ankri, D. Fixler, Nanophotonics 2017, 6, 1031.
- 107J. T. Robinson, K. Welsher, S. M. Tabakman, S. P. Sherlock, H. Wang, R. Luong, H. Dai, Nano Res. 2010, 3, 779.
- 108O. Betzer, R. Ankri, M. Motiei, R. Popovtzer, J. Nanomater. 2015, 2015, 1.
- 109E. C. Dreaden, M. A. Mackey, X. Huang, B. Kang, M. A. El-Sayed, Chem. Soc. Rev. 2011, 40, 3391.
- 110J. Lin, S. Wang, P. Huang, Z. Wang, S. Chen, G. Niu, W. Li, J. He, D. Cui, G. Lu, X. Chen, Z. Nie, ACS Nano 2013, 7, 5320.
- 111R. K. Kramer, N. Pholchai, V. J. Sorger, T. J. Yim, R. Oulton, X. Zhang, Nanotechnology 2010, 21, 145307.
- 112D. Fixler, T. Nayhoz, K. Ray, ACS Photonics 2014, 1, 900.
- 113J. Zong, S. L. Cobb, N. R. Cameron, Biomater. Sci. 2017, 5, 872.
- 114Q. Jiang, Z.-G. Wang, B. Ding, Small 2013, 9(9), 1016.
- 115Z. Hu, J. Ma, F. Fu, C. Cui, X. Li, X. Wang, W. Wang, Y. Wan, Z. Yuan, J. Control. Release 2017, 268, 1.
- 116K. Suhling, J. Siegel, P. M. P. Lanigan, S. Lévêque-Fort, S. E. D. Webb, D. Phillips, D. M. Davis, P. M. W. French, Opt. Lett. 2004, 29, 584.
- 117J. R. Lakowicz, H. Szmacinski, K. Nowaczyk, K. W. Berndt, M. Johnson, Anal. Biochem. 1992, 202, 316.
- 118M. Y. Berezin, S. Achilefu, Chem. Rev. 2010, 110, 2641.
- 119D. M. Jameson, J. A. Ross, Chem. Rev. 2010, 110, 2685.
- 120J. A. Dix, A. S. Verkman, Biophys. J. 1990, 57, 231.
- 121R. J. Cherry, Biochim. Biophys. Acta - Rev. Biomembr. 1979, 559, 289.
- 122D. S. Smith, S. A. Eremin, Anal. Bioanal. Chem. 2008, 391, 1499.
- 123J. R. Lakowicz, I. Gryczynski, H. Szmacinski, H. Cherek, N. Joshi, Eur. Biophys. J. 1991, 19, 125.
- 124D. S. Lidke, P. Nagy, B. G. Barisas, R. Heintzmann, J. N. Post, K. A. Lidke, A. H. A. Clayton, D. J. Arndt-Jovin, T. M. Jovin, Biochem. Soc. Trans. 2003, 31, 1020.
- 125A. Le Marois, S. Labouesse, K. Suhling, R. Heintzmann, J. Biophotonics 2017, 10, 1124.
- 126L. D. Lavis, R. T. Raines, ACS Chem. Biol. 2014, 9, 855.
- 127D. Fixler, R. Tirosh, T. Zinman, A. Shainberg, M. Deutsch, Cell Calcium 2002, 31(6), 279.
- 128N. Zurgil, Y. Shafran, D. Fixler, M. Deutsch, Biochem. Biophys. Res. Commun. 2002, 290(5), 1573.