Genetic targeting of a small fluorescent zinc indicator to cell surface for monitoring zinc secretion

ACS Chemical Biology

Volumn 10, Issue 4, 2015, Pages 1054-1063

  Li, Daliang ^a,b   Liu, Lin ^a   Li, Wen Hong ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b FUJIAN NORMAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; FLUORESCENT DYE; INSULIN; PROTEIN TAG; ZINC; RECOMBINANT PROTEIN;

AMINATION; AMINO ACID SEQUENCE; ARTICLE; CELL LABELING; CELL MEMBRANE; CELL ORGANELLE; CELL SURFACE; CELL TRACKING; CELLULAR SECRETION; CONJUGATION; CONTROLLED STUDY; COVALENT BOND; EXOCYTOSIS; FLUORESCENCE MICROSCOPY; GENE TARGETING; INSULIN RELEASE; MEMBRANE DEPOLARIZATION; MEMBRANE FUSION; MYRISTYLATION; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEOPHILICITY; OPTOGENETICS; PANCREAS ISLET BETA CELL; PARACRINE SIGNALING; PHOTOACTIVATION; PHOTOSTIMULATION; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; SECRETORY CELL; STIMULUS SECRETION COUPLING; ANIMAL; CELL LINE; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR GENETICS; MOUSE; NUCLEOTIDE SEQUENCE; PROCEDURES; PROTEIN ENGINEERING; SYNTHESIS; ULTRAVIOLET SPECTROPHOTOMETRY;

ANIMALIA; MAMMALIA;

ANIMALS; BASE SEQUENCE; CELL LINE; CELL MEMBRANE; CHEMISTRY TECHNIQUES, SYNTHETIC; FLUORESCENT DYES; INSULIN; MICE; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; OPTOGENETICS; PROTEIN ENGINEERING; RECOMBINANT PROTEINS; SPECTROPHOTOMETRY, ULTRAVIOLET; ZINC;

EID: 84928122081     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb5007536     Document Type: Article

References (42)

1. Rorsman, P. and Braun, M. (2013) Regulation of insulin secretion in human pancreatic islets Annu. Rev. Physiol. 75, 155-179
2. Sudhof, T. C. and Rothman, J. E. (2009) Membrane fusion: grappling with SNARE and SM proteins Science 323, 474-477
3. Burgess, T. L. and Kelly, R. B. (1987) Constitutive and regulated secretion of proteins Annu. Rev. Cell Biol. 3, 243-293
4. Rutter, G. A., Varadi, A., Tsuboi, T., Parton, L., and Ravier, M. (2006) Insulin secretion in health and disease: genomics, proteomics and single vesicle dynamics Biochem. Soc. Trans. 34, 247-250
5. Lin, W. J. and Salton, S. R. (2013) The regulated secretory pathway and human disease: insights from gene variants and single nucleotide polymorphisms Front. Endocrinol. 4, 96
6. Li, W. H. and Li, D. (2013) Fluorescent probes for monitoring regulated secretion Curr. Opin. Chem. Biol. 17, 672-681
7. Frederickson, C. J., Koh, J. Y., and Bush, A. I. (2005) The neurobiology of zinc in health and disease Nat. Rev. Neurosci. 6, 449-462
8. Li, D., Chen, S., Bellomo, E. A., Tarasov, A. I., Kaut, C., Rutter, G. A., and Li, W. H. (2011) Imaging dynamic insulin release using a fluorescent zinc indicator for monitoring induced exocytotic release (ZIMIR) Proc. Natl. Acad. Sci. U.S.A. 108, 21063-21068
9. Tarasov, A. I., Semplici, F., Li, D., Rizzuto, R., Ravier, M. A., Gilon, P., and Rutter, G. A. (2012) Frequency-dependent mitochondrial Ca(2+) accumulation regulates ATP synthesis in pancreatic beta cells Pflugers Arch. 465, 543-554
10. Hodson, D. J., Mitchell, R. K., Bellomo, E. A., Sun, G., Vinet, L., Meda, P., Li, D., Li, W. H., Bugliani, M., Marchetti, P., Bosco, D., Piemonti, L., Johnson, P., Hughes, S. J., and Rutter, G. A. (2013) Lipotoxicity disrupts incretin-regulated human beta cell connectivity J. Clin. Invest. 123, 4182-4194
11. Hodson, D. J., Mitchell, R. K., Marselli, L., Pullen, T. J., Brias, S. G., Semplici, F., Everett, K. L., Cooper, D. M., Bugliani, M., Marchetti, P., Lavallard, V., Bosco, D., Piemonti, L., Johnson, P. R., Hughes, S. J., Li, D., Li, W. H., Shapiro, A. M., and Rutter, G. A. (2014) ADCY5 couples glucose to insulin secretion in human islets Diabetes 63, 3009-3021
12. Los, G. V., Encell, L. P., McDougall, M. G., Hartzell, D. D., Karassina, N., Zimprich, C., Wood, M. G., Learish, R., Ohana, R. F., Urh, M., Simpson, D., Mendez, J., Zimmerman, K., Otto, P., Vidugiris, G., Zhu, J., Darzins, A., Klaubert, D. H., Bulleit, R. F., and Wood, K. V. (2008) HaloTag: a novel protein labeling technology for cell imaging and protein analysis ACS Chem. Biol. 3, 373-382
13. Hinner, M. J. and Johnsson, K. (2010) How to obtain labeled proteins and what to do with them Curr. Opin. Biotechnol. 21, 766-776
14. Wu, J., Liu, L., Matsuda, T., Zhao, Y., Rebane, A., Drobizhev, M., Chang, Y. F., Araki, S., Arai, Y., March, K., Hughes, T. E., Sagou, K., Miyata, T., Nagai, T., Li, W. H., and Campbell, R. E. (2013) Improved orange and red Ca indicators and photophysical considerations for optogenetic applications ACS Chem. Neurosci. 4, 963-972
15. Encell, L. P., Friedman Ohana, R., Zimmerman, K., Otto, P., Vidugiris, G., Wood, M. G., Los, G. V., McDougall, M. G., Zimprich, C., Karassina, N., Learish, R. D., Hurst, R., Hartnett, J., Wheeler, S., Stecha, P., English, J., Zhao, K., Mendez, J., Benink, H. A., Murphy, N., Daniels, D. L., Slater, M. R., Urh, M., Darzins, A., Klaubert, D. H., Bulleit, R. F., and Wood, K. V. (2012) Development of a dehalogenase-based protein fusion tag capable of rapid, selective and covalent attachment to customizable ligands Curr. Chem. Genomics 6, 55-71
16. Hong, H., Benink, H. A., Zhang, Y., Yang, Y., Uyeda, H. T., Engle, J. W., Severin, G. W., McDougall, M. G., Barnhart, T. E., Klaubert, D. H., Nickles, R. J., Fan, F., and Cai, W. (2011) HaloTag: a novel reporter gene for positron emission tomography Am. J. Transl. Res. 3, 392-403
17. Zhang, X. A., Song, D., and Lippard, S. J. (2008) A reversible pH-dependent intramolecular pyridine-aldehyde cyclization J. Org. Chem. 73, 734-737
18. Bernstein, J. G., Garrity, P. A., and Boyden, E. S. (2012) Optogenetics and thermogenetics: technologies for controlling the activity of targeted cells within intact neural circuits Curr. Opin. Neurobiol. 22, 61-71
19. Alford, S. C., Wu, J., Zhao, Y., Campbell, R. E., and Knopfel, T. (2013) Optogenetic reporters Biol. Cell. 105, 14-29
20. Berndt, A., Schoenenberger, P., Mattis, J., Tye, K. M., Deisseroth, K., Hegemann, P., and Oertner, T. G. (2011) High-efficiency channelrhodopsins for fast neuronal stimulation at low light levels Proc. Natl. Acad. Sci. U.S.A. 108, 7595-7600
21. Iyoshi, S., Taki, M., and Yamamoto, Y. (2011) Development of a cholesterol-conjugated fluorescent sensor for site-specific detection of zinc ion at the plasma membrane Org. Lett. 13, 4558-4561
22. Radford, R. J., Chyan, W., and Lippard, S. J. (2013) Peptide-based targeting of fluorescent zinc sensors to the plasma membrane of live cells Chem. Sci. 4, 3080-3084
23. Vinkenborg, J. L., Nicolson, T. J., Bellomo, E. A., Koay, M. S., Rutter, G. A., and Merkx, M. (2009) Genetically encoded FRET sensors to monitor intracellular Zn2+ homeostasis Nat. Methods 6, 737-740
24. Qin, Y., Dittmer, P. J., Park, J. G., Jansen, K. B., and Palmer, A. E. (2011) Measuring steady-state and dynamic endoplasmic reticulum and Golgi Zn2+ with genetically encoded sensors Proc. Natl. Acad. Sci. U.S.A. 108, 7351-7356
25. Vinkenborg, J. L., Koay, M. S., and Merkx, M. (2010) Fluorescent imaging of transition metal homeostasis using genetically encoded sensors Curr. Opin. Chem. Biol. 14, 231-237
26. Carter, K. P., Young, A. M., and Palmer, A. E. (2014) Fluorescent sensors for measuring metal ions in living systems Chem. Rev. 114, 4564-4601
27. Masharina, A., Reymond, L., Maurel, D., Umezawa, K., and Johnsson, K. (2012) A Fluorescent Sensor for GABA and Synthetic GABA(B) Receptor Ligands J. Am. Chem. Soc. 134, 19026-19034
28. Kosaka, N., Ogawa, M., Choyke, P. L., Karassina, N., Corona, C., McDougall, M., Lynch, D. T., Hoyt, C. C., Levenson, R. M., Los, G. V., and Kobayashi, H. (2009) In vivo stable tumor-specific painting in various colors using dehalogenase-based protein-tag fluorescent ligands Bioconjugate Chem. 20, 1367-1374
29. So, M. K., Yao, H., and Rao, J. (2008) HaloTag protein-mediated specific labeling of living cells with quantum dots Biochem. Biophys. Res. Commun. 374, 419-423
30. Svendsen, S., Zimprich, C., McDougall, M. G., Klaubert, D. H., and Los, G. V. (2008) Spatial separation and bidirectional trafficking of proteins using a multi-functional reporter BMC Cell Biol. 9, 17
31. Tomat, E., Nolan, E. M., Jaworski, J., and Lippard, S. J. (2008) Organelle-specific zinc detection using zinpyr-labeled fusion proteins in live cells J. Am. Chem. Soc. 130, 15776-15777
32. Reiner, T., Thurber, G., Gaglia, J., Vinegoni, C., Liew, C. W., Upadhyay, R., Kohler, R. H., Li, L., Kulkarni, R. N., Benoist, C., Mathis, D., and Weissleder, R. (2011) Accurate measurement of pancreatic islet β-cell mass using a second-generation fluorescent exendin-4 analog Proc. Natl. Acad. Sci. U.S.A. 108, 12815-12820
33. Speier, S., Nyqvist, D., Cabrera, O., Yu, J., Molano, R. D., Pileggi, A., Moede, T., Kohler, M., Wilbertz, J., Leibiger, B., Ricordi, C., Leibiger, I. B., Caicedo, A., and Berggren, P. O. (2008) Noninvasive in vivo imaging of pancreatic islet cell biology Nat. Med. 14, 574-578
34. Coppieters, K., Amirian, N., and von Herrath, M. (2012) Intravital imaging of CTLs killing islet cells in diabetic mice J. Clin. Invest. 119-131
35. Lubag, A. J., De Leon-Rodriguez, L. M., Burgess, S. C., and Sherry, A. D. (2011) Noninvasive MRI of beta-cell function using a Zn2+-responsive contrast agent Proc. Natl. Acad. Sci. U.S.A. 108, 18400-18405
36. Dakin, K., Zhao, Y. R., and Li, W. H. (2005) LAMP, a new imaging assay of gap junctional communication unveils that Ca2+ influx inhibits cell coupling Nat. Methods 2, 55-62
37. Dakin, K. and Li, W. H. (2006) Infrared-LAMP: two-photon uncaging and imaging of gap junctional communication in three dimensions Nat. Methods 3, 959
38. Govorunova, E. G., Sineshchekov, O. A., Li, H., Janz, R., and Spudich, J. L. (2013) Characterization of a highly efficient blue-shifted channelrhodopsin from the marine alga Platymonas subcordiformis J. Biol. Chem. 288, 29911-29922
39. Klapoetke, N. C., Murata, Y., Kim, S. S., Pulver, S. R., Birdsey-Benson, A., Cho, Y. K., Morimoto, T. K., Chuong, A. S., Carpenter, E. J., Tian, Z., Wang, J., Xie, Y., Yan, Z., Zhang, Y., Chow, B. Y., Surek, B., Melkonian, M., Jayaraman, V., Constantine-Paton, M., Wong, G. K., and Boyden, E. S. (2014) Independent optical excitation of distinct neural populations Nat. Methods 11, 338-346
40. Unger, R. H. and Orci, L. (2010) Paracrinology of islets and the paracrinopathy of diabetes Proc. Natl. Acad. Sci. U.S.A. 107, 16009-16012
41. Walker, J. N., Ramracheya, R., Zhang, Q., Johnson, P. R., Braun, M., and Rorsman, P. (2011) Regulation of glucagon secretion by glucose: paracrine, intrinsic or both? Diabetes, Obes. Metab. 13 (Suppl 1) 95-105
42. Cigliola, V., Chellakudam, V., Arabieter, W., and Meda, P. (2013) Connexins and beta-cell functions Diabetes Res. Clin. Pract. 99, 250-259