ACTIVATABLE SMART PROBES FOR MOLECULAR OPTICAL IMAGING AND THERAPY

JONATHAN F. LOVELL; GANG ZHENG

[1] Bai, Y., Zhang, B., Xu, J., Duan, C., Dang, D., Liu, D. and Meng, Q. “Conformational switching fluorescent chemosensor for chloride anion,” New. J. Chem. 29, 777–779 (2005).

[2] Belousov, V. V., Fradkov, A. F., Lukyanov, K. A., Staroverov, D. B., Shakhbazov, K. S., Terskikh, A. V. and Lukyanov, S. “Genetically encoded fluorescent indicator for intracellular hydrogen peroxide,” Nat. Methods 3, 281–286 (2006).

[3] Blum, G., von Degenfeld, G., Merchant, M. J., Blau, H. M. and Bogyo, M. “Noninvasive optical imaging of cysteine protease activity using fluorescently quenched activity-based probes,” Nat. Chem. Biol. 3, 668–677 (2007).

[4] Bratu, D. P., Cha, B., Mhlanga, M. M., Kramer, F. R. and Tyagi, S. “Visualizing the distribution and transport of mRNAs in living cells,” Proc. Natl. Acad. Sci. USA 100, 13308–13313 (2003).

[5] Chen, J., Stefflova, K., Niedre, M. J., Wilson, B. C., Chance, B., Glickson, J. D. and Zheng, G. “Protease-triggered photosensitizing beacon based on singlet oxygen quenching and activation, J. Am. Chem. Soc. 126, 11450–11451 (2004).

[6] Chudakov, D. M., Lukyanov, S. and Lukyanov, K. A. “Fluorescent proteins as a toolkit for in vivo imaging,” Trends Biotechnol. 23, 605–613 (2005).

[7] Cui, Z., Zhang, Z., Zhang, X.,Wen, J., Zhou, Y. and Xie, W. “Visualizing the dynamic behavior of poliovirus plus-strand RNA in living host cells,” Nucleic. Acids. Res. 33, 3245–3252 (2005).

[8] Dong, M., Tepp, W. H., Johnson, E. A. and Chapman, E. R. “Using fluorescent sensors to detect botulinum neurotoxin activity in vitro and in living cells,” Proc. Natl. Acad. Sci. USA 101, 14701–14706 (2004).

[9] Dunphy, I., Vinogradov, S. A. and Wilson, D. F. “Oxyphor R2 and G2: phosphors for measuring oxygen by oxygen-dependent quenching of phosphorescence,” Anal. Biochem. 310, 191–198 (2002).

[10] Farber, S. A., Pack, M., Ho, S. Y., Johnson, I. D., Wagner, D. S., Dosch, R., Mullins, M. C., Hendrickson, H. S., Hendrickson, E. K. and Halpern, M. E. “Genetic analysis of digestive physiology using fluorescent phospholipid reporters,” Science 292, 1385– 1388 (2001).

[11] Fehr, M., Frommer, W. B. and Lalonde, S. “Visualization of maltose uptake in living yeast cells by fluorescent nanosensors,” Proc. Natl. Acad. Sci. USA 99, 9846–9851 (2002).

[12] Flors, C., Fryer, M. J., Waring, J., Reeder, B., Bechtold, U., Mullineaux, P. M., Nonell, S., Wilson, M. T. and Baker, N. R. “Imaging the production of singlet oxygen in vivo using a new fluorescent sensor, Singlet Oxygen Sensor Green,” J. Exp. Bot. 57, 1725–1734 (2006).

[13] Funovics, M., Weissleder, R. and Tung, C. “Protease sensors for bioimaging,” Anal. Bioanal. Chem. 377, 956–963 (2003).

[14] Gee, K. R., Zhou, Z., Qian, W. and Kennedy, R. “Detection and imaging of zinc secretion from pancreatic beta-cells using a new fluorescent zinc indicator,” J. Am. Chem. Soc. 124, 776–778 (2002).

[15] Giepmans, B. N. G., Adams, S. R., Ellisman, M. H. and Tsien, R. Y. “The fluorescent toolbox for assessing protein location and function,” Science 312, 217–224 (2006).

[16] Godavarty, A., Sevick-Muraca, E. M. and Eppstein, M. J. “Three-dimensional fluorescence lifetime tomography,” Med. Phys. 32, 992–1000 (2005).

[17] Goel, G., Kumar, A., Puniya, A. K., Chen, W. and Singh, K. “Molecular beacon: a multitask probe,” J. Appl. Microbiol. 99, 435–442 (2005).

[18] Grynkiewicz, G., Poenie, M. and Tsien, R. Y. “A new generation of Ca2+ indicators with greatly improved fluorescence properties,” J. Biol. Chem. 260, 3440–3450 (1985).

[19] Gurskaya, N. G., Verkhusha, V. V., Shcheglov, A. S., Staroverov, D. B., Chepurnykh, T.V., Fradkov,A. F., Lukyanov, S. and Lukyanov,K. A. “Engineering of amonomeric green-to-red photoactivatable fluorescent protein induced by blue light,” Nat. Biotechnol. 24, 461–465 (2006).

[20] Hara, M., Bindokas, V., Lopez, J. P., Kaihara, K., Landa, L. R., Harbeck, M. and Roe, M. W. “Imaging endoplasmic reticulum calcium with a fluorescent biosensor in transgenic mice,” Am. J. Physiol. Cell Physiol. 287, C932–C938 (2004).

[21] Hideg, E., Barta, C., K′alai, T., Vass, I., Hideg, K. and Asada, K. “Detection of singlet oxygen and superoxide with fluorescent sensors in leaves under stress by photoinhibition or UV radiation,” Plant Cell Physiol. 43, 1154–1164 (2002).

[22] Hu, C., Chinenov, Y. and Kerppola, T. K. “Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation,” Mol. Cell 9, 789–798 (2002).

[23] Jaffer, F. A., Kim, D., Quinti, L., Tung, C., Aikawa, E., Pande, A. N., Kohler, R. H., Shi, G., Libby, P. and Weissleder, R. “Optical visualization of cathepsin K activity in atherosclerosis with a novel, protease-activatable fluorescence sensor,” Circulation 115, 2292–2298 (2007).

[24] Jiang, T., Olson, E. S., Nguyen, Q. T., Roy, M., Jennings, P. A. and Tsien, R. Y. “Tumor imaging by means of proteolytic activation of cell-penetrating peptides,” Proc. Natl. Acad. Sci. USA 101, 17867–17872 (2004).

[25] Johnson, I. “Fluorescent probes for living cells,” Histochem. J. 30, 123–140 (1998).

[26] Kay, A. R. “Evidence for chelatable zinc in the extracellular space of the hippocampus, but little evidence for synaptic release of Zn,” J. Neurosci. 23, 6847–6855 (2003).

[27] Kim, Y., Choi, Y., Weissleder, R. and Tung, C. “Membrane permeable esteraseactivated fluorescent imaging probe,” Bioorg. Med. Chem. Lett. 17, 5054–5057 (2007).

[28] Kojima, H., Nakatsubo, N., Kikuchi, K., Kawahara, S., Kirino, Y., Nagoshi, H., Hirata, Y. and Nagano, T. “Detection and imaging of nitric oxide with novel fluorescent indicators: diaminofluoresceins,” Anal. Chem. 70, 2446–2453 (1998).

[29] Kwon, J. Y., Jang, Y. J., Lee, Y. J., Kim, K. M., Seo, M. S., Nam, W. and Yoon, J. “A highly selective fluorescent chemosensor for Pb2+,” J. Am. Chem. Soc. 127, 10107–10111 (2005).

[30] Lee, D., Khaja, S., Velasquez-Castano, J. C., Dasari, M., Sun, C., Petros, J., Taylor, W. R. and Murthy, N. “In vivo imaging of hydrogen peroxide with chemiluminescent nanoparticles,” Nat. Mater. 6, 765–769 (2007).

[31] Lin, J., Zhang, Z., Yang, J., Zeng, S., Liu, B. and Luo, Q. “Real-time detection of caspase-2 activation in a single living HeLa cell during cisplatin-induced apoptosis,” J. Biomed. Opt. 11, 024011 (2006).

[32] Lin, Z., Xie, L., Zhao, Y., Duan, C. and Qu, J. “Thiourea-based molecular clips for fluorescent discrimination of isomeric dicarboxylates,” Org. Biomol. Chem. 5, 3535– 3538 (2007).

[33] Liu, L., Yermolaieva, O., Johnson, W. A., Abboud, F. M. and Welsh, M. J. “Identification and function of thermosensory neurons in Drosophila larvae,” Nat. Neurosci. 6, 267–273 (2003).

[34] Lu, J., Zhang, Z., Yang, J., Chu, J., Li, P., Zeng, S. and Luo, Q. “Visualization of beta-secretase cleavage in living cells using a genetically encoded surface-displayed FRET probe,” Biochem. Biophys. Res. Commun. 362, 25–30 (2007).

[35] Mahmood, U., Tung, C. H., Bogdanov, A. and Weissleder, R. “Near-infrared optical imaging of protease activity for tumor detection,” Radiology 213, 866–870 (1999).

[36] Massoud, T. F. and Gambhir, S. S. “Molecular imaging in living subjects: seeing fundamental biological processes in a new light,” Genes. Dev. 17, 545–580 (2003).

[37] McIntyre, J. O., Fingleton, B., Wells, K. S., Piston, D. W., Lynch, C. C., Gautam, S. and Matrisian, L. M. “Development of a novel fluorogenic proteolytic beacon for in vivo detection and imaging of tumour-associated matrix metalloproteinase-7 activity,” Biochem. J. 377, 617–628 (2004).

[38] Meade, T. J., Taylor, A. K. and Bull, S. R. “New magnetic resonance contrast agents as biochemical reporters,” Curr. Opin. Neurobiol. 13, 597–602 (2003).

[39] Miesenb¨ock, G., Angelis, D. A. D. and Rothman, J. E. “Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins,” Nature 394, 192– 195 (1998).

[40] Miller, E. W., Tulyathan, O., Tulyanthan, O., Isacoff, E. Y. and Chang, C. J. “Molecular imaging of hydrogen peroxide produced for cell signaling,” Nat. Chem. Biol. 3, 263–267 (2007).

[41] Mitra, R. D., Silva, C. M. and Youvan, D. C. “Fluorescence resonance energy transfer between blue-emitting and red-shifted excitation derivatives of the green fluorescent protein,” Gene 173, 13–17 (1996).

[42] Miyawaki, A., Llopis, J., Heim, R., McCaffery, J. M., Adams, J. A., Ikura, M. and Tsien, R. Y. “Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin,” Nature 388, 882–887 (1997).

[43] Moerner, W. E. “New directions in single-molecule imaging and analysis,” Proc. Natl. Acad. Sci. USA 104, 12596–12602 (2007).

[44] Molenaar, C., Marras, S. A., Slats, J. C., Truffert, J. C., Lema tre, M., Raap, A. K., Dirks, R. W. and Tanke, H. J. “Linear 2’ O-Methyl RNA probes for the visualization of RNA in living cells,” Nucleic. Acids Res. 29, E89–E89 (2001).

[45] Moschou, E. A., Sharma, B. V., Deo, S. K. and Daunert, S. “Fluorescence glucose detection: advances toward the ideal in vivo biosensor,” J. Fluoresc. 14, 535–547 (2004).

[46] Nesterov, E. E., Skoch, J., Hyman, B. T., Klunk, W. E., Bacskai, B. J. and Swager, T. M. “In vivo optical imaging of amyloid aggregates in brain: design of fluorescent markers,” Angew. Chem. Int. Ed. Engl. 44, 5452–5456 (2005).

[47] Ntziachristos, V., Tung, C., Bremer, C. and Weissleder, R. “Fluorescence molecular tomography resolves protease activity in vivo,” Nat. Med. 8, 757–760 (2002).

[48] Ntziachristos, V., Yodh, A. G., Schnall, M. and Chance, B. “Concurrent MRI and diffuse optical tomography of breast after indocyanine green enhancement,” Proc. Natl. Acad. Sci. USA 97, 2767–2772 (2000).

[49] O’Riordan, T. C., Fitzgerald, K., Ponomarev, G. V., Mackrill, J., Hynes, J., Taylor, C. and Papkovsky, D. B. “Sensing intracellular oxygen using near-infrared phosphorescent probes and live-cell fluorescence imaging,” Am. J. Physiol. Regul. Integr. Comp. Physiol. 292, R1613–R1620 (2007).

[50] Oleinick, N. L. and Evans, H. H. “The photobiology of photodynamic therapy: cellular targets and mechanisms,” Radiat. Res. 150, S146–S156 (1998).

[51] Patterson, G. H. and Lippincott-Schwartz, J. “A photoactivatable GFP for selective photolabeling of proteins and cells,” Science 297, 1873–1877 (2002).

[52] Peter, M. and Ameer-Beg, S. M. “Imaging molecular interactions by multiphoton FLIM,” Biol. Cell 96, 231–236 (2004).

[53] Petrat, F., Weisheit, D., Lensen, M., de Groot, H., Sustmann, R. and Rauen, U. “Selective determination of mitochondrial chelatable iron in viable cells with a new fluorescent sensor,” Biochem. J. 362, 137–147 (2002).

[54] Post, J. N., Lidke, K. A., Rieger, B. and Arndt-Jovin, D. J. “One- and two-photon photoactivation of a paGFP-fusion protein in live Drosophila embryos,” FEBS Lett. 579, 325–330 (2005).

[55] Ramanujan, V. K., Zhang, J., Biener, E. and Herman, B. “Multiphoton fluorescence lifetime contrast in deep tissue imaging: prospects in redox imaging and disease diagnosis,” J. Biomed. Opt. 10, 051407 (2005).

[56] Richards-Kortum, R. and Sevick-Muraca, E. “Quantitative optical spectroscopy for tissue diagnosis,” Annu. Rev. Phys. Chem. 47, 555–606 (1996).

[57] Russell, J., Diamond, K., Collins, T., Weston M., Lovell J., Hayward, J., Farrell, T., Patterson, M. and Fang, Q. “Characterization of time-domain fluorescence properties of typical photosensitizers for photodynamic therapy,” Proc. SPIE 6437, 64270G1-9 (2007).

[58] Sando, S., Abe, H. and Kool, E. T. “Quenched auto-ligating DNAs: multicolor identification of nucleic acids at single nucleotide resolution,” J. Am. Chem. Soc. 126, 1081–1087 (2004).

[59] Santangelo, P. J., Nix, B., Tsourkas, A. and Bao, G. “Dual FRET molecular beacons for mRNA detection in living cells,” Nucleic. Acids. Res. 32, e57 (2004).

[60] Skala, M. C., Riching, K. M., Bird, D. K., Gendron-Fitzpatrick, A., Eickhoff, J., Eliceiri, K. W., Keely, P. J. and Ramanujam, N. “In vivo multiphoton fluorescence lifetime imaging of protein-bound and free nicotinamide adenine dinucleotide in normal and precancerous epithelia,” J. Biomed. Opt. 12, 024014 (2007).

[61] Stefflova, K., Chen, J. and Zheng, G. “Killer beacons for combined cancer imaging and therapy,” Curr. Med. Chem. 14, 2110–2125 (2007).

[62] Stefflova, K., Chen, J. and Zheng, G. “Using molecular beacons for cancer imaging and treatment,” Frontiers in Bioscience 12, 4709–4721 (2007).

[63] Tan, W., Wang, K. and Drake, T. J. “Molecular beacons,” Curr. Opin. Chem. Biol. 8, 547–553 (2004).

[64] Truong, K., Sawano, A., Mizuno, H., Hama, H., Tong, K., Mal, T., Miyawaki, A. and Ikura, M. “FRET-based in vivo Ca2+ imaging by a new calmodulin-GFP fusion molecule,” Nat. Struct. Biol. 8, 1069–1073 (2001).

[65] Tung, C., Zeng, Q., Shah, K., Kim, D., Schellingerhout, D. and Weissleder, R. “In vivo imaging of beta-galactosidase activity using far red fluorescent switch,” Cancer Res. 64, 1579–1583 (2004).

[66] Tyagi, S. and Kramer, F. R. “Molecular beacons: probes that fluoresce upon hybridization,” Nat. Biotechnol. 14, 303–308 (1996).

[67] Vargas, D. Y., Raj, A., Marras, S. A. E., Kramer, F. R. and Tyagi, S. “Mechanism of mRNA transport in the nucleus,” Proc. Natl. Acad. Sci. USA 102, 17008–17013 (2005).

[68] Wehrman, T. S., von Degenfeld, G., Krutzik, P. O., Nolan, G. P. and Blau, H. M. “Luminescent imaging of beta-galactosidase activity in living subjects using sequential reporter-enzyme luminescence,” Nat. Methods 3, 295–301 (2006).

[69] Weissleder, R., Tung, C. H., Mahmood, U. and Bogdanov, A. “In vivo imaging of tumors with protease-activated near-infrared fluorescent probes,” Nat. Biotechnol. 17, 375–378 (1999).

[70] Xi, C., Balberg, M., Boppart, S. A. and Raskin, L. “Use of DNA and peptide nucleic acid molecular beacons for detection and quantification of rRNA in solution and in whole cells,” Appl. Environ. Microbiol. 69, 5673–5678 (2003).

[71] Yang, L., McRae, R., Henary, M. M., Patel, R., Lai, B., Vogt, S. and Fahrni, C. J. “Imaging of the intracellular topography of copper with a fluorescent sensor and by synchrotron x-ray fluorescence microscopy,” Proc. Natl. Acad. Sci. USA 102, 11179– 11184 (2005).

[72] Yasui, H. and Sakurai, H. “Chemiluminescent detection and imaging of reactive oxygen species in live mouse skin exposed to UVA,” Biochem. Biophys. Res. Commun. 269, 131–136 (2000).

[73] Zhang, J., Ma, Y., Taylor, S. S. and Tsien, R. Y. “Genetically encoded reporters of protein kinase A activity reveal impact of substrate tethering,” Proc. Natl. Acad. Sci. USA 98, 14997–15002 (2001).

[74] Zhang, Z., Yang, J., Lu, J., Lin, J., Zeng, S. and Luo, Q. “Fluorescence imaging to assess the matrix metalloproteinase activity and its inhibitor in vivo,” J. Biomed. Opt. 13, 011006 (2008).

[75] Zheng, G., Chen, J., Stefflova, K., Jarvi, M., Li, H. and Wilson, B. C. “Photodynamic molecular beacon as an activatable photosensitizer based on protease-controlled singlet oxygen quenching and activation,” Proc. Natl. Acad. Sci. USA 104, 8989–8994 (2007).

[76] Zipfel, W. R., Williams, R. M. and Webb, W. W. “Nonlinear magic: multiphoton microscopy in the biosciences,” Nat. Biotechnol. 21, 1369–1377 (2003).