Labeling Acetyl- and Butyrylcholinesterase Using Semiconductor Nanocrystals for Biological Applications

BioNanoScience

Volumn 3, Issue 1, 2013, Pages 1-11

  Waiskopf, Nir ^a   Rotem, Rany ^a   Shweky, Itzhak ^a   Yedidya, Lior ^a   Soreq, Hermona ^a   Banin, Uri ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Acetylcholinesterase; Anticholinesterases; Bioconjugation; Butyrylcholinesterase; Imaging; Quantum dots; Quantum rods

Indexed keywords

BIOLOGICAL SYSTEMS; FLUORESCENCE; GRAPHENE QUANTUM DOTS; IMAGING TECHNIQUES; MEDICAL APPLICATIONS; NANOCRYSTALS; PHOTOBLEACHING; SEMICONDUCTOR QUANTUM DOTS; SIGNAL TRANSDUCTION;

ACETYLCHOLINESTERASE; ANTICHOLINESTERASES; BIO-CONJUGATION; BUTYRYLCHOLINESTERASE; QUANTUM RODS;

ENZYMES;

5, 5' DITHIOBIS (2 NITROBENZOIC ACID); ACETYLCHOLINESTERASE; CHOLINESTERASE; QUANTUM DOT; RECOMBINANT ENZYME; UNCLASSIFIED DRUG;

ADSORPTION; AGAR GEL ELECTROPHORESIS; ANIMAL CELL; ARTICLE; CELL VIABILITY; COLORIMETRY; CONFOCAL MICROSCOPY; CONJUGATION; CYTOTOXICITY; ENZYME STRUCTURE; FLUORESCENCE MICROSCOPY; HUMAN; INFRARED SPECTROPHOTOMETRY; NONHUMAN; SYNTHESIS; TRANSMISSION ELECTRON MICROSCOPY; ULTRAVIOLET SPECTROPHOTOMETRY;

EID: 84873510531     PISSN: 21911630     EISSN: 21911649     Source Type: Journal    
DOI: 10.1007/s12668-012-0072-3     Document Type: Article

References (74)

1. Medintz, I. L., Uyeda, H. T., Goldman, E. R., Mattoussi, H. (2005). Quantum dot bioconjugates for imaging, labelling and sensing. Nature Materials, 4(6), 435-446.
2. Resch-Genger, U., Grabolle, M., Cavaliere-Jaricot, S., Nitschke, R., Nann, T. (2008). Quantum dots versus organic dyes as fluorescent labels. Nature Methods, 5(9), 763-775.
3. Mattoussi, H., Palui, G., Na, H. B. (2012). Luminescent quantum dots as platforms for probing in vitro and in vivo biological processes. Advanced Drug Delivery Reviews, 64(2), 138-166.
4. Rosenthal, S. J., Chang, J. C., Kovtun, O., McBride, J. R., Tomlinson, I. D. (2011). Biocompatible quantum dots for biological applications. Chemical Biology, 18(1), 10-24.
5. Yu, W. W., Qu, L., Guo, W., Peng, X. (2003). Experimental determination of the extinction coefficient of CdTe, CdSe, and CdS nanocrystals. Chemistry of Materials, 15(14), 2854-2860.
6. Leatherdale, C. A., Woo, W. K., Mikulec, F. V., Bawendi, M. G. (2002). On the absorption cross section of CdSe nanocrystal quantum dots. The Journal of Physical Chemistry B, 106(31), 7619-7622.
7. Larson, D. R., Zipfel, W. R., Williams, R. M., Clark, S. W., Bruchez, M. P., Wise, F. W., Webb, W. W. (2003). Water-soluble quantum dots for multiphoton fluorescence imaging in vivo. Science, 300(5624), 1434-1436.
8. Delehanty, J. B., Bradburne, C. E., Susumu, K., Boeneman, K., Mei, B. C., Farrell, D., Blanco-Canosa, J. B., Dawson, P. E., Mattoussi, H., Medintz, I. L. (2011). Spatiotemporal multicolor labeling of individual cells using peptide-functionalized quantum dots and mixed delivery techniques. Journal of the American Chemical Society, 133(27), 10482-10489.
9. Sun, Y. H., Liu, Y. S., Vernier, P. T., Liang, C. H., Chong, S. Y., Marcu, L., Gundersen, M. A. (2006). Photostability and pH sensitivity of CdSe/ZnSe/ZnS quantum dots in living cells. Nanotechnology, 17(17), 4469-4476.
10. Nida, D. L., Nitin, N., Yu, W. W., Colvin, V. L., Richards-Kortum, R. (2008). Photostability of quantum dots with amphiphilic polymer-based passivation strategies. Nanotechnology, 19(3), 035701.
11. Wu, X. Y., Liu, H. J., Liu, J. Q., Haley, K. N., Treadway, J. A., Larson, J. P., Ge, N. F., Peale, F., Bruchez, M. P. (2003). Immunofluorescent labeling of cancer marker Her2 and other cellular targets with semiconductor quantum dots. Nature Biotechnology, 21(1), 41-46.
12. Kovtun, O., Tomlinson, I. D., Sakrikar, D. S., Chang, J. C., Blakely, R. D., Rosenthal, S. J. (2011). Visualization of the cocaine-sensitive dopamine transporter with ligand-conjugated quantum dots. ACS Chemical Neuroscience, 2(7), 370-378.
13. Chang, J. C., Tomlinson, I. D., Warnement, M. R., Ustione, A., Carneiro, A. M. D., Piston, D. W., Blakely, R. D., Rosenthal, S. J. (2012). Single molecule analysis of serotonin transporter regulation using antagonist-conjugated quantum dots reveals restricted, p38 MAPK-dependent mobilization underlying uptake activation. Journal of Neuroscience, 32(26), 8919-8929.
14. Freeman, R., & Willner, I. (2012). Optical molecular sensing with semiconductor quantum dots (QDs). Chemical Society Reviews, 41(10), 4067-4085.
15. Smith, A. M., Duan, H. W., Mohs, A. M., Nie, S. M. (2008). Bioconjugated quantum dots for in vivo molecular and cellular imaging. Advanced Drug Delivery Reviews, 60(11), 1226-1240.
16. Hermanson, G. T. (1996). Bioconjugate techniques. New York: Academic.
17. Darvesh, S., Hopkins, D. A., Geula, C. (2003). Neurobiology of butyrylcholinesterase. Nature Reviews Neuroscience, 4(2), 131-138.
18. Soreq, H., & Seidman, S. (2001). Acetylcholinesterase-New roles for an old actor. Nature Reviews Neuroscience, 2(4), 294-302.
19. Taylor, P. (1996). Agents acting at the neuromuscular junction and autonomic ganglia. In J. Hardman, L. Limbird, P. Molinoff, R. Ruddon (Eds.), Goodman and Gilman's the pharmacological basis of therapeutics (9th ed., pp. 177-197). New York: McGraw-Hill.
20. Sklan, E. H., Lowenthal, A., Korner, M., Ritov, Y., Landers, D. M., Rankinen, T., Bouchard, C., Leon, A. S., Rice, T., Rao, D. C., Wilmore, J. H., Skinner, J. S., Soreq, H. (2004). Acetylcholinesterase/paraoxonase genotype and expression predict anxiety scores in health, risk factors, exercise training, and genetics study. Proceedings of the National Academy of Sciences of the United States of America, 101(15), 5512-5517.
21. Ofek, K., Schoknecht, K., Melamed-Book, N., Heinemann, U., Friedman, A., Soreq, H. (2012). Fluoxetine induces vasodilation of cerebral arterioles by co-modulating NO/muscarinic signaling. Journal of Cellular and Molecular Medicine. doi: 10. 1111/j. 1582-4934. 2012. 01596. x.
22. Ofek, K., Krabbe, K. S., Evron, T., Debecco, M., Nielsen, A. R., Brunnsgaad, H., Yirmiya, R., Soreq, H., Pedersen, B. K. (2007). Cholinergic status modulations in human volunteers under acute inflammation. Journal of Molecular Medicine (Berlin), 85(11), 1239-1251.
23. Pottie, I. R., Higgins, E. A., Blackman, R. A., Macdonald, I. R., Martin, E., Darvesh, S. (2011). Cysteine thioesters as myelin proteolipid protein analogues to examine the role of butyrylcholinesterase in myelin decompaction. ACS Chemical Neuroscience, 2(3), 151-159.
24. Valle, A., O'Connor, D. T., Taylor, P., Zhu, G., Montgomery, G. W., Slagboom, P. E., Martin, N. G., Whitfield, J. B. (2006). Butyrylcholinesterase: Association with the metabolic syndrome and identification of 2 gene loci affecting activity. Clinical Chemistry, 52(6), 1014-1020.
25. Layer, P. (1995). Nonclassical roles of cholinesterases in the embryonic brain and possible links to Alzheimer disease. Alzheimer Disease and Associated Disorders, 9, 29-36.
26. Podoly, E., Shalev, D. E., Shenhar-Tsarfaty, S., Bennett, E. R., Ben Assayag, E., Wilgus, H., Livnah, O., Soreq, H. (2009). The butyrylcholinesterase K variant confers structurally derived risks for Alzheimer pathology. Journal of Biological Chemistry, 284(25), 17170-17179.
27. Shenhar-Tsarfaty, S., Bruck, T., Bennett, E. R., Bravman, T., Aassayag, E. B., Waiskopf, N., Rogowski, O., Bornstein, N., Berliner, S., Soreq, H. (2011). Butyrylcholinesterase interactions with amylin may protect pancreatic cells in metabolic syndrome. Journal of Cellular and Molecular Medicine, 15(8), 1747-1756.
28. Geula, C., & Mesulam, M. (1989). Special properties of cholinesterases in the cerebral cortex of Alzheimer's disease. Brain Research, 498(1), 185-189.
29. Benmoyal-Segal, L., Vander, T., Shifman, S., Bryk, B., Ebstein, R. P., Marcus, E.-L., Stessman, J., Darvasi, A., Herishanu, Y., Friedman, A., Soreq, H. (2005). Acetylcholinesterase/paraoxonase interactions increase the risk of insecticide-induced Parkinson's disease. The FASEB Journal, 19(3), 452-454.
30. Ben Assayag, E., Shenhar-Tsarfaty, S., Ofek, K., Soreq, L., Bova, I., Shopin, L., Berg, R. M., Berliner, S., Shapira, I., Bornstein, N. M., Soreq, H. (2010). Serum cholinesterase activities distinguish between stroke patients and controls and predict 12-month mortality. Molecular Medicine, 16(7-8), 278-286.
31. Canaani, J., Shenhar-Tsarfaty, S., Waiskopf, N., Yakobi, R., Ben Assayag, E., Berliner, S., Soreq, H. (2010). Serum AChE activities predict exercise heart rate parameters of asymptomatic individuals. Neuroscience & Medicine, 1(2), 43-49.
32. Brenner, T., Hamra-Amitay, Y., Evron, T., Boneva, N., Seidman, S., Soreq, H. (2003). The role of readthrough acetylcholinesterase in the pathophysiology of myasthenia gravis. The FASEB Journal, 17(2), 214-222.
33. Geyer, B. C., Kannan, L., Garnaud, P. E., Broomfield, C. A., Cadieux, C. L., Cherni, I., Hodgins, S. M., Kasten, S. A., Kelley, K., Kilbourne, J., Oliver, Z. P., Otto, T. C., Puffenberger, I., Reeves, T. E., Robbins, N., 2nd, Woods, R. R., Soreq, H., Lenz, D. E., Cerasoli, D. M., Mor, T. S. (2010). Plant-derived human butyrylcholinesterase, but not an organophosphorous-compound hydrolyzing variant thereof, protects rodents against nerve agents. Proceedings of the National Academy of Sciences of the United States of America, 107(47), 20251-20256.
34. Geyer, B. C., Muralidharan, M., Cherni, I., Doran, J., Fletcher, S. P., Evron, T., Soreq, H., Mor, T. S. (2005). Purification of transgenic plant-derived recombinant human acetylcholinesterase-R. Chemico-Biological Interactions, 157-158, 331-334.
35. Hai, A., Ben-Haim, D., Korbakov, N., Cohen, A., Shappir, J., Oren, R., Spira, M. E., Yitzchaik, S. (2006). Acetylcholinesterase-ISFET based system for the detection of acetylcholine and acetylcholinesterase inhibitors. Biosensors and Bioelectronics, 22(5), 605-612.
36. Liu, G., Wang, J., Barry, R., Petersen, C., Timchalk, C., Gassman, P. L., Lin, Y. (2008). Nanoparticle-based electrochemical immunosensor for the detection of phosphorylated acetylcholinesterase: An exposure biomarker of organophosphate pesticides and nerve agents. Chemistry, 14(32), 9951-9959.
37. Pardo-Yissar, V., Katz, E., Wasserman, J., Willner, I. (2003). Acetylcholine esterase-labeled CdS nanoparticles on electrodes: Photoelectrochemical sensing of the enzyme inhibitors. Journal of the American Chemical Society, 125(3), 622-623.
38. Evron, T., Geyer, B. C., Cherni, I., Muralidharan, M., Kilbourne, J., Fletcher, S. P., Soreq, H., Mor, T. S. (2007). Plant-derived human acetylcholinesterase-R provides protection from lethal organophosphate poisoning and its chronic aftermath. The FASEB Journal, 21(11), 2961-2969.
39. Mazor, O., Cohen, O., Kronman, C., Raveh, L., Stein, D., Ordentlich, A., Shafferman, A. (2008). Aging-resistant organophosphate bioscavenger based on polyethylene glycol-conjugated F338A human acetylcholinesterase. Molecular Pharmacology, 74(3), 755-763.
40. Johnson, N. D., Duysen, E. G., Lockridge, O. (2009). Intrathecal delivery of fluorescent labeled butyrylcholinesterase to the brains of butyrylcholinesterase knock-out mice: Visualization and quantification of enzyme distribution in the brain. Neurotoxicology, 30(3), 386-392.
41. Gaydess, A., Duysen, E., Li, Y., Gilman, V., Kabanov, A., Lockridge, O., Bronich, T. (2011). Visualization of exogenous delivery of nanoformulated butyrylcholinesterase to the central nervous system. Chemico-Biological Interactions, 187(1-3), 295-298.
42. Waiskopf, N., Shweky, I., Lieberman, I., Banin, U., Soreq, H. (2011). Quantum dot labeling of butyrylcholinesterase maintains substrate and inhibitor interactions and cell adherence features. ACS Chemical Neuroscience, 2(3), 141-150.
43. Buiculescu, R., Hatzimarinaki, M., Chaniotakis, N. A. (2010). Biosilicated CdSe/ZnS quantum dots as photoluminescent transducers for acetylcholinesterase-based biosensors. Analytical and Bioanalytical Chemistry, 398(7-8), 3015-3021.
44. Wang, H., Wang, J., Timchalk, C., Lin, Y. (2008). Magnetic electrochemical immunoassays with quantum dot labels for detection of phosphorylated acetylcholinesterase in plasma. Analytical Chemistry, 80(22), 8477-8484.
45. Zhang, L. W., & Monteiro-Riviere, N. A. (2009). Mechanisms of quantum dot nanoparticle cellular uptake. Toxicological Sciences, 110(1), 138-155.
46. Chang, E., Thekkek, N., Yu, W. W., Colvin, V. L., Drezek, R. (2006). Evaluation of quantum dot cytotoxicity based on intracellular uptake. Small, 2(12), 1412-1417.
47. Hu, J., Li, L., Yang, W., Manna, L., Wang, L., Alivisatos, A. P. (2001). Linearly polarized emission from colloidal semiconductor quantum rods. Science, 292(5524), 2060-2063.
48. Ohmachi, M., Komori, Y., Iwane, A. H., Fujii, F., Jin, T., Yanagida, T. (2012). Fluorescence microscopy for simultaneous observation of 3D orientation and movement and its application to quantum rod-tagged myosin V. Proceedings of the National Academy of Sciences of the United States of America, 109(14), 5294-5298.
49. Carbone, L., Nobile, C., De Giorgi, M., Sala, F. D., Morello, G., Pompa, P., Hytch, M., Snoeck, E., Fiore, A., Franchini, I. R., Nadasan, M., Silvestre, A. F., Chiodo, L., Kudera, S., Cingolani, R., Krahne, R., Manna, L. (2007). Synthesis and micrometer-scale assembly of colloidal CdSe/CdS nanorods prepared by a seeded growth approach. Nano Letters, 7(10), 2942-2950.
50. Peng, X. G., Schlamp, M. C., Kadavanich, A. V., Alivisatos, A. P. (1997). Epitaxial growth of highly luminescent CdSe/CdS core/shell nanocrystals with photostability and electronic accessibility. Journal of the American Chemical Society, 119(30), 7019-7029.
51. Yin, Y., & Alivisatos, A. P. (2005). Colloidal nanocrystal synthesis and the organic-inorganic interface. Nature, 437(7059), 664-670.
52. Lees, E. E., Nguyen, T.-L., Clayton, A. H. A., Mulvaney, P., Muir, B. W. (2009). The preparation of colloidally stable, water-soluble, biocompatible, semiconductor nanocrystals with a small hydrodynamic diameter. ACS Nano, 3(5), 1121-1128.
53. Geidel, C., Schmachtel, S., Riedinger, A., Pfeiffer, C., Mullen, K., Klapper, M., Parak, W. J. (2011). A general synthetic approach for obtaining cationic and anionic inorganic nanoparticles via encapsulation in amphiphilic copolymers. Small, 7(20), 2929-2934.
54. Zhang, F., Lees, E., Amin, F., Gil, P. R., Yang, F., Mulvaney, P., Parak, W. J. (2011). Polymer-coated nanoparticles: A universal tool for biolabelling experiments. Small, 7(22), 3113-3127.
55. Hoshino, A., Fujioka, K., Oku, T., Suga, M., Sasaki, Y. F., Ohta, T., Yasuhara, M., Suzuki, K., Yamamoto, K. (2004). Physicochemical properties and cellular toxicity of nanocrystal quantum dots depend on their surface modification. Nano Letters, 4(11), 2163-2169.
56. Sperling, R. A., & Parak, W. J. (2010). Surface modification, functionalization and bioconjugation of colloidal inorganic nanoparticles. Philosophical Transactions. Series A, Mathematical, Physical, and Engineering Sciences, 368(1915), 1333-1383.
57. Derjaguin, B., & Landau, L. (1993). Theory of the stability of strongly charged lyophobic sols and of the adhesion of strongly charged-particles in solutions of electrolytes. Progress in Surface Science, 43(1-4), 30-59.
58. Smith, A. M., Duan, H. W., Rhyner, M. N., Ruan, G., Nie, S. M. (2006). A systematic examination of surface coatings on the optical and chemical properties of semiconductor quantum dots. Physical Chemistry Chemical Physics, 8(33), 3895-3903.
59. Clift, M. J. D., Boyles, M. S. P., Brown, D. M., Stone, V. (2010). An investigation into the potential for different surface-coated quantum dots to cause oxidative stress and affect macrophage cell signalling in vitro. Nanotoxicology, 4(2), 139-149.
60. Mittal, R., & Bruchez, M. P. (2011). Biotin-4-fluorescein based fluorescence quenching assay for determination of biotin binding capacity of streptavidin conjugated quantum dots. Bioconjugate Chemistry, 22(3), 362-368.
61. Medintz, I. L., Pons, T., Susumu, K., Boeneman, K., Dennis, A. M., Farrell, D., Deschamps, J. R., Melinger, J. S., Bao, G., Mattoussi, H. (2009). Resonance energy transfer between luminescent quantum dots and diverse fluorescent protein acceptors. Journal of Physical Chemistry C Nanomaterials and Interfaces, 113(43), 18552-18561.
62. Mosmann, T. (1983). Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. Journal of Immunological Methods, 65(1-2), 55-63.
63. Sperling, R. A., Pellegrino, T., Li, J. K., Chang, W. H., Parak, W. J. (2006). Electrophoretic separation of nanoparticles with a discrete number of functional groups. Advanced Functional Materials, 16(7), 943-948.
64. Baker, N. A., Sept, D., Joseph, S., Holst, M. J., McCammon, J. A. (2001). Electrostatics of nanosystems: Application to microtubules and the ribosome. Proceedings of the National Academy of Sciences of the United States of America, 98(18), 10037-10041.
65. Wang, Z., Zhao, J., Li, F., Gao, D., Xing, B. (2009). Adsorption and inhibition of acetylcholinesterase by different nanoparticles. Chemosphere, 77(1), 67-73.
66. Wang, Z., Zhang, K., Zhao, J., Liu, X., Xing, B. (2010). Adsorption and inhibition of butyrylcholinesterase by different engineered nanoparticles. Chemosphere, 79(1), 86-92.
67. Janczewski, D., Tomczak, N., Han, M. Y., Vancso, G. J. (2011). Synthesis of functionalized amphiphilic polymers for coating quantum dots. Nature Protocols, 6(10), 1546-1553.
68. Perrier, A. L., Massoulie, J., Krejci, E. (2002). PRiMA: The membrane anchor of acetylcholinesterase in the brain. Neuron, 33(2), 275-285.
69. Sussman, J. D., Argov, Z., McKee, D., Hazum, E., Brawer, S., Soreq, H. (2008). Antisense treatment for myasthenia gravis: Experience with monarsen. Annals of the New York Academy of Sciences, 1132, 283-290.
70. Ellman, G. L., Courtney, K. D., Andres, V., Featherstone, R. M. (1961). A new and rapid colorimetric determination of acetylcholinesterase activity. Biochemical Pharmacology, 7(2), 88-95.
71. Ngamelue, M. N., Homma, K., Lockridge, O., Asojo, O. A. (2007). Crystallization and X-ray structure of full-length recombinant human butyrylcholinesterase. Acta Crystallographica. Section F, Structural Biology and Crystallization Communications, 63, 723-727.
72. Dvir, H., Silman, I., Harel, M., Rosenberry, T. L., Sussman, J. L. (2010). Acetylcholinesterase: From 3D structure to function. Chemico-Biological Interactions, 187(1-3), 10-22.
73. Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T. N., Weissig, H., Shindyalov, I. N., Bourne, P. E. (2000). The protein data bank. Nucleic Acids Research, 28(1), 235-242.
74. Dolinsky, T. J., Nielsen, J. E., McCammon, J. A., Baker, N. A. (2004). PDB2PQR: An automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations. Nucleic Acids Research, 32(Web Server issue), W665-W667.