Biochemistry of mobile zinc and nitric oxide revealed by fluorescent sensors

Annual Review of Biochemistry

Volumn 80, Issue , 2011, Pages 333-355

  Pluth, Michael D ^a   Tomat, Elisa ^a   Lippard, Stephen J ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

cell imaging; fluorescent probes

Indexed keywords

1,2 DIAMINOANTHRAQUINONE; 2,3 NAPHTHALENEDIAMINE; 6 METHOXY 8 4 TOLUENESULFONAMIDEQUINOLINE; ARYLTRIAZOLE; DI(2 PICOLYL)AMINE; DIAMINOFLUORESCEIN; FLUORESCENT DYE; GREEN FLUORESCENT PROTEIN; NITRIC OXIDE; NITROSAMINE; QUINOLINE DERIVATIVE; RHODAMINE; TRANSITION ELEMENT; TRIAZOLE DERIVATIVE; UNCLASSIFIED DRUG; ZINC; ZINC (II); ZINPYR; ZINQUIN A; ZINQUIN E;

ALZHEIMER DISEASE; APOPTOSIS; ARTICLE; BIOSENSOR; CARDIOVASCULAR SYSTEM; CHEMICAL STRUCTURE; FLUORESCENCE ANALYSIS; FLUORESCENCE IMAGING; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; IMMUNE DEFICIENCY; IMMUNE SYSTEM; INTRACELLULAR SIGNALING; MOLECULAR INTERACTION; MOLECULAR PROBE; NERVOUS SYSTEM; NEUROPATHOLOGY; NEUROTOXICITY; NITROSATION; NONHUMAN; PRIORITY JOURNAL; STEREOCHEMISTRY; VASOCONSTRICTION;

ANIMALS; BIOSENSING TECHNIQUES; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENT DYES; HUMANS; MOLECULAR STRUCTURE; NITRIC OXIDE; SIGNAL TRANSDUCTION; ZINC;

EID: 79959404630     PISSN: 00664154     EISSN: 00664154     Source Type: Book Series    
DOI: 10.1146/annurev-biochem-061009-091643     Document Type: Article

References (156)

1. Andreini C, Banci L, Bertini I, Rosato A. 2006. Counting the zinc-proteins encoded in the human genome. J. Proteome Res. 5:196-201. (Pubitemid 43100813)
2. Sousa SF, Lopes AB, Fernandes PA, Ramos MJ. 2009. The zinc proteome: a tale of stability and functionality. Dalton Trans. (38):7946-956.
3. Maret W, Li Y. 2009. Coordination dynamics of zinc in proteins. Chem. Rev. 109:4682-707.
4. Lichten LA, Cousins RJ. 2009. Mammalian zinc transporters: nutritional and physiologic regulation. Annu. Rev. Nutr. 29:153-176.
5. Maret W. 2000. The function of zinc metallothionein: a link between cellular zinc and redox state. J. Nutr. 130:S1455-458.
6. Vallee BL, Falchuk KH. 1993. The biochemical basis of zinc physiology. Physiol. Rev. 73:79-118. (Pubitemid 23065434)
7. Maret W, Krȩżel A. 2007. Cellular zinc and redox buffering capacity of metallothionein/thionein in health and disease. Mol. Med. 13:371-375. (Pubitemid 47378138)
8. Frederickson CJ, Koh J-Y, Bush AI. 2005. The neurobiology of zinc in health and disease. Nat. Rev. Neurosci. 6:449-462. (Pubitemid 40774861)
9. Takeda A, Tamano H. 2009. Insight into zinc signaling from dietary zinc deficiency. Brain Res. Rev. 62:33-44.
10. Kay AR, T́oth K. 2008. Is zinc a neuromodulator? Sci. Signal. 1:re3.
11. Sensi SL, Paoletti P, Bush AI, Sekler I. 2009. Zinc in the physiology and pathology of the CNS. Nat. Rev. Neurosci. 10:780-791.
12. Taylor CG. 2005. Zinc, the pancreas, and diabetes: insights from rodent studies and future directions. BioMetals 18:305-312. (Pubitemid 41298013)
13. Jansen J, Karges W, Rink L. 2009. Zinc and diabetes-clinical links and molecular mechanisms. J. Nutr. Biochem. 20:399-417.
14. Wijesekara N, Chimienti F, Wheeler MB. 2009. Zinc, a regulator of islet function and glucose homeostasis. Diabetes Obes. Metab. 11:202-214.
15. Costello LC, Franklin RB. 2006. The clinical relevance of the metabolism of prostate cancer; zinc and tumor suppression: connecting the dots. Mol. Cancer 5:17.
16. Franklin RB, Costello LC. 2007. Zinc as an antitumor agent in prostate cancer and in other cancers. Arch. Biochem. Biophys. 463:211-217. (Pubitemid 47030335)
17. Costello LC, Franklin RB. 2009. Prostatic fluid electrolyte composition for the screening of prostate cancer: a potential solution to a major problem. Prostate Cancer Prostatic Dis. 12:17-24.
18. Ghosh SK, Kim P, Zhang X-A, Yun S-H, Moore A, et al. 2010. A novel imaging approach for early detection of prostate cancer based on endogenous zinc sensing. Cancer Res. 70:6119-127.
19. Ignarro LJ, Buga GM, Wood KS, Byrns RE, Chaudhuri G. 1987. Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc. Natl. Acad. Sci. USA 84:9265-269.
20. Palmer RMJ, Ferrige AG, Moncada S. 1987. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 327:524-526. (Pubitemid 17085822)
21. Marletta MA, Yoon PS, Iyengar R, Leaf CD, Wishnok JS. 1988. Macrophage oxidation of L-arginine to nitrite and nitrate: Nitric oxide is an intermediate. Biochemistry 27:8706-711. (Pubitemid 19008186)
22. Bredt DS, Hwang PM, Snyder SH. 1990. Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature 347:768-770.
23. Shibuki K, Okada D. 1991. Endogenous nitric oxide release required for long-term synaptic depression in the cerebellum. Nature 349:326-328. (Pubitemid 21912074)
24. Loscalzo J, Welch G. 1995. Nitric oxide and its role in the cardiovascular system. Prog. Cardiovasc. Dis. 38:87-104.
25. Bogdan C. 2001. Nitric oxide and the immune response. Nat. Immunol. 2:907-916. (Pubitemid 32976162)
26. Fukumura D, Kashiwagi S, Jain RK. 2006. The role of nitric oxide in tumour progression. Nat. Rev. Cancer 6:521-534. (Pubitemid 43980541)
27. Garthwaite J. 2008. Concepts of neural nitric oxide-mediated transmission. Eur. J. Neurosci. 27:2783-802. (Pubitemid 351832227)
28. Gladwin MT, Schechter AN, Kim-Shapiro DB, Patel RP, Hogg N, et al. 2005. The emerging biology of the nitrite anion. Nat. Chem. Biol. 1:308-314.
29. Bryan NS. 2006. Nitrite in nitric oxide biology: Cause or consequence? A systems-based review. Free Radic. Biol. Med. 41:691-701. (Pubitemid 44163410)
30. Johnson RA, Freeman RH. 1992. Sustained hypertension in the rat induced by chronic blockade of nitric oxide production. Am. J. Hypertens. 5:919-922. (Pubitemid 23022579)
31. Weis M, Kledal TN, Lin KY, Panchal SN, Gao SZ, et al. 2004. Cytomegalovirus infection impairs the nitric oxide synthase pathway: role of asymmetric dimethylarginine in transplant arteriosclerosis. Circulation 109:500-5. (Pubitemid 38168513)
32. Rajfer J, Aronson WJ, Bush PA, Dorey FJ, Ignarro LJ. 1992. Nitric oxide as a mediator of relaxation of the corpus cavernosum in response to nonadrenergic, noncholinergic neurotransmission. N. Engl. J. Med. 326:90-94.
33. Pieper GM. 1998. Review of alterations in endothelial nitric oxide production in diabetes: protective role of arginine on endothelial dysfunction. Hypertension 31:1047-060. (Pubitemid 28191496)
34. Oyadomari S, Takeda K, Takiguchi M, Gotoh T, Matsumoto M, et al. 2001. Nitric oxide-induced apoptosis in pancreatic βcells is mediated by the endoplasmic reticulum stress pathway. Proc. Natl. Acad. Sci. USA 98:10845-850. (Pubitemid 32878707)
35. Chan PH. 2001. Reactive oxygen radicals in signaling and damage in the ischemic brain. J. Cereb. Blood Flow Metab. 21:2-14. (Pubitemid 32036708)
36. Titheradge MA. 1999. Nitric oxide in septic shock. Biochim. Biophys. Acta 1411:437-455. (Pubitemid 29221966)
37. Smith KJ, Lassmann H. 2002. The role of nitric oxide in multiple sclerosis. Lancet Neurol. 1:232-241. (Pubitemid 37159185)
38. Hussain SP, Hofseth LJ, Harris CC. 2003. Radical causes of cancer. Nat. Rev. Cancer 3:276-285. (Pubitemid 37328863)
39. Heales SJR, Bolãnos JP, Stewart VC, Brookes PS, Land JM, Clark JB. 1999. Nitric oxide, mitochondria and neurological disease. Biochim. Biophys. Acta 1410:215-228. (Pubitemid 29078606)
40. Brown GC, Bal-Price A. 2003. Inflammatory neurodegeneration mediated by nitric oxide, glutamate, and mitochondria. Mol. Neurobiol. 27:325-355. (Pubitemid 38156291)
41. Fukuto JM, Dutton AS, Houk KN. 2005. The chemistry and biology of nitroxyl (HNO): a chemically unique species with novel and important biological activity. ChemBioChem 6:612-619. (Pubitemid 40873757)
42. Szab́o C, Ischiropoulos H, Radi R. 2007. Peroxynitrite: biochemistry, pathophysiology and development of therapeutics. Nat. Rev. Drug Discov. 6:662-680. (Pubitemid 47207751)
43. Kikuchi K, Komatsu K, Nagano T. 2004. Zinc sensing for cellular application. Curr. Opin. Chem. Biol. 8:182-191. (Pubitemid 38452434)
44. Jiang P, Guo Z. 2004. Fluorescent detection of zinc in biological systems: recent development on the design of chemosensors and biosensors. Coord. Chem. Rev. 248:205-229.
45. Carol P, Sreejith S, AjayaghoshA. 2007. Ratiometric and near-infraredmolecular probes for the detection and imaging of zinc ions. Chem. Asian J. 2:338-348.
46. Domaille DW, Que EL, Chang CJ. 2008. Synthetic fluorescent sensors for studying the cell biology of metals. Nat. Chem. Biol. 4:168-175. (Pubitemid 351265326)
47. McRae R, Bagchi P, Sumalekshmy S, Fahrni CJ. 2009. In situ imaging of metals in cells and tissues. Chem. Rev. 109:4780-827.
48. Nolan EM, Lippard SJ. 2009. Small-molecule fluorescent sensors for investigating zinc metalloneurochemistry. Acc. Chem. Res. 42:193-203.
49. Tomat E, Lippard SJ. 2010. Imaging mobile zinc in biology. Curr. Opin. Chem. Biol. 14:225-230.
50. Vinkenborg JL, Koay MS, Merkx M. 2010. Fluorescent imaging of transition metal homeostasis using genetically encoded sensors. Curr. Opin. Chem. Biol. 14:231-237.
51. 2+/GSK-3β signal pathway in cardiomyocytes. Am. J. Physiol. Heart Circ. Physiol. 298:H601-7.
52. Ghafourifar P, Parihar MS, Nazarewicz R, Zenebe WJ, Parihar A. 2008. Detection assays for determination of mitochondrial nitric oxide synthase activity; advantages and limitations. Methods Enzymol. 440:317-334.
53. Gomes A, Fernandes E, Lima JLFC. 2006. Use of fluorescence probes for detection of reactive nitrogen species: a review. J. Fluoresc. 16:119-139.
54. Hetrick EM, Schoenfisch MH. 2009. Analytical chemistry of nitric oxide. Annu. Rev. Anal. Chem. 2:409-33.
55. Hong H, Sun J, Cai W. 2009. Multimodality imaging of nitric oxide and nitric oxide synthases. Free Radic. Biol. Med. 47:684-698.
56. McQuade LE, Lippard SJ. 2010. Fluorescent probes to investigate nitric oxide and other reactive nitrogen species in biology. Curr. Opin. Chem. Biol. 14:43-49.
57. Nagano T. 2009. Bioimaging probes for reactive oxygen species and reactive nitrogen species. J. Clin. Biochem. Nutr. 45:111-124.
58. Nagano T, Yoshimura T. 2002. Bioimaging of nitric oxide. Chem. Rev. 102:1235-269. (Pubitemid 35377609)
59. Wardman P. 2007. Fluorescent and luminescent probes for measurement of oxidative and nitrosative species in cells and tissues: progress, pitfalls, and prospects. Free Radic. Biol. Med. 43:995-1022. (Pubitemid 47302656)
60. Ye X, Rubakhin SS, Sweedler JV. 2008. Detection of nitric oxide in single cells. Analyst 133:423-433. (Pubitemid 351441966)
61. Mahanand D, Houck JC. 1968. Fluorometric determination of zinc in biologic fluids. Clin. Chem. 14:6-11.
62. Smith GL, Jenkins RA, Gough JF. 1969. A fluorescent method for the detection and localization of zinc in human granulocytes. J. Histochem. Cytochem. 17:749-750.
63. Frederickson CJ, Kasarskis EJ, Ringo D, Frederickson RE. 1987. A quinoline fluorescence method for visualizing and assaying the histochemically reactive zinc (bouton zinc) in the brain. J. Neurosci. Methods 20:91-103. (Pubitemid 17091479)
64. Zalewski PD, Millard SH, Forbes IJ, Kapaniris O, Slavotinek A, et al. 1994. Video image analysis of labile zinc in viable pancreatic islet cells using a specific fluorescent probe for zinc. J. Histochem. Cytochem. 42:877-884. (Pubitemid 24198446)
65. Fahrni CJ, O'Halloran TV. 1999. Aqueous coordination chemistry of quinoline-based fluorescence probes for the biological chemistry of zinc. J. Am. Chem. Soc. 121:11448-458.
66. 2+ based on a fluorescein platform: synthesis, properties and intracellular distribution. J. Am. Chem. Soc. 123:7831-841. (Pubitemid 32899347)
67. 2+ sensors. J. Am. Chem. Soc. 131:7142-152.
68. 2+ sensor Zinpyr-1: a computational investigation. J. Phys. Chem. A 114:10427-434.
69. Wong BA, Fredle S, Lippard SJ. 2009. Subtle modification of 2, 2-dipicolylamine lowers the affinity and improves the turn-on of Zn(II)-selective fluorescent sensors. Inorg. Chem. 48:7009-011.
70. 2+. Chem. Soc. Rev. 39:1996-2006.
71. Nolan EM, Ryu JW, Jaworski J, Feazell RP, Sheng M, Lippard SJ. 2006. Zinspy sensors with enhanced dynamic range for imaging neuronal cell zinc uptake and mobilization. J. Am. Chem. Soc. 128:15517-528. (Pubitemid 44876028)
72. Nolan EM, Jaworski J, Okamoto K-I, Hayashi Y, Sheng M, Lippard SJ. 2005. QZ1 and QZ2: rapid, reversible quinoline-derivatized fluoresceins for sensing biological Zn(II). J. Am. Chem. Soc. 127:16812-23. (Pubitemid 41772842)
73. Zhang X-A, Hayes D, Smith SJ, Friedle S, Lippard SJ. 2008. New strategy for quantifying biological zinc by a modified Zinpyr fluorescence sensor. J. Am. Chem. Soc. 130:15788-789.
74. Hirano T, Kikuchi K, Urano Y, Higuchi T, Nagano T. 2000. Highly zinc-selective fluorescent sensor molecules suitable for biological applications. J. Am. Chem. Soc. 122:12399-400. (Pubitemid 32062289)
75. 2+ in hippocampal slices. J. Am. Chem. Soc. 127:10197-204. (Pubitemid 41045485)
76. Haugland RP. 2002. Handbook of Fluorescent Probes and Research Products. Eugene, OR: Molecular Probes. 919 pp.
77. 2+-selective, cell-permeable, and ratiometric fluorescent sensor. J. Am. Chem. Soc. 132:601-610.
78. Gee KR, Zhou Z-L, Qian W-J, Kennedy R. 2002. Detection and imaging of zinc secretion from pancreatic β-cells using a new fluorescent zinc indicator. J. Am. Chem. Soc. 124:776-778. (Pubitemid 34112786)
79. Zhao J, Bertoglio BA, Gee KR, Kay AR. 2008. The zinc indicator FluoZin-3 is not perturbed significantly by physiological levels of calcium or magnesium. Cell Calcium 44:422-426.
80. Du P, Lippard SJ. 2010. A highly selective turn-on colorimetric, red fluorescent sensor for detecting mobile zinc in living cells. Inorg. Chem. 49:10753-755.
81. Tomat E, Lippard SJ. 2010. Ratiometric and intensity-based zinc sensors built on rhodol and rhodamine platforms. Inorg. Chem. 49:9113-115.
82. Komatsu K, Urano Y, Kojima H, Nagano T. 2007. Development of an iminocoumarin-based zinc sensor suitable for ratiometric fluorescence imaging of neuronal zinc. J. Am. Chem. Soc. 129:13447-454. (Pubitemid 350071772)
83. 2+ using a rhodamine spirolactam as a trigger. Anal. Chem. 82:3108-113.
84. Dittmer PJ, Miranda JG, Gorski JA, Palmer AE. 2009. Genetically encoded sensors to elucidate spatial distribution of cellular zinc. J. Biol. Chem. 284:16289-297.
85. 2+ homeostasis. Nat. Methods 6:737-740.
86. Marks KM, Nolan GP. 2006. Chemical labeling strategies for cell biology. Nat. Methods 3:591-596. (Pubitemid 44123423)
87. Johnsson N, Johnsson K. 2007. Chemical tools for biomolecular imaging. ACS Chem. Biol. 2:31-38. (Pubitemid 47490240)
88. Keppler A, Gendreizig S, Gronemeyer T, Pick H, Vogel H, Johnsson K. 2003. A general method for the covalent labeling of fusion proteins with small molecules in vivo. Nat. Biotechnol. 21:86-89. (Pubitemid 36055833)
89. Tomat E, Nolan EM, Jaworski J, Lippard SJ. 2008. Organelle-specific zinc detection using Zinpyrlabeled fusion proteins in live cells. J. Am. Chem. Soc. 130:15776-777.
90. Hornig FS, Korth H-G, Rauen U, de Groot H, Sustmann R. 2006. Synthesis and properties of a pHinsensitive fluorescent nitric oxide cheletropic trap (FNOCT). Helv. Chim. Acta 89:2281-296. (Pubitemid 44745761)
91. Meineke P, Rauen U, de Groot H, Korth H-G, Sustmann R. 2000. Nitric oxide detection and visualization in biological systems. Applications of the FNOCT method. Biol. Chem. 381:575-582. (Pubitemid 30657880)
92. Meineke P, Rauen U, de Groot H, Korth H-G, Sustmann R. 1999. Cheletropic traps for the fluorescence spectroscopic detection of nitric oxide (nitrogen monoxide) in biological systems. Chem. Eur. J. 5:1738-47. (Pubitemid 129611593)
93. Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR. 1982. Analysis of nitrate, nitrite, and [N-15]-labeled nitrate in biological-fluids. Anal. Biochem. 126:131-138. (Pubitemid 13203451)
94. Griess P. 1879. Bemerkungen zu der abhandlung der HH. Weselky und benedikt ueber einige azoverbindungen. Ber. Dtsch. Chem. Ges. 12:426-428.
95. Nagano T, Takizawa H, Hirobe M. 1995. Reactions of nitric oxide with amines in the presence of dioxygen. Tetrahedron Lett. 36:8239-242.
96. Misko TP, Schilling RJ, Salvemini D, Moore WM, Currie MG. 1993. A fluorometric assay for the measurement of nitrite in biological samples. Anal. Biochem. 214:11-16. (Pubitemid 23300346)
97. Marzinzig M, Nussler AK, Stadler J, Marzinzig E, Barthlen W, et al. 1997. Improved methods to measure end products of nitric oxide in biological fluids: nitrite, nitrate, and S-nitrosothiols. Nitric Oxide 1:177-189. (Pubitemid 28076558)
98. Kojima H, Nakatsubo N, Kikuchi K, Urano Y, Higuchi T, et al. 1998. Direct evidence ofNOproduction in rat hippocampus and cortex using a new fluorescent indicator: DAF-2 DA. NeuroReport 9:3345-348. (Pubitemid 28566108)
99. Kojima H, Nakatsubo N, Kikuchi K, Kawahara S, Kirino Y, et al. 1998. Detection and imaging of nitric oxide with novel fluorescent indicators: diaminofluoresceins. Anal. Chem. 70:2446-453.
100. Nakatsubo N, Kojima H, Kikuchi K, Nagoshi H, Hirata Y, et al. 1998. Direct evidence of nitric oxide production from bovine aortic endothelial cells using new fluorescence indicators: diaminofluoresceins. FEBS Lett. 427:263-266. (Pubitemid 28225070)
101. Kim W-S, Ye XY, Rubakhin SS, Sweedler JV. 2006. Measuring nitric oxide in single neurons by capillary electrophoresis with laser-induced fluorescence: use of ascorbate oxidase in diaminofluorescein measurements. Anal. Chem. 78:1859-865.
102. Zhang X, Kim WS, Hatcher N, Potgieter K, Moroz LL, et al. 2010. Interfering with nitric oxide measurements: 4, 5-diaminofluorescein reacts with dehydroascorbic acid and ascorbic acid. J. Biol. Chem. 277:48472-478.
103. Broillet M-C, Randin O, Chatton J-Y. 2001. Photoactivation and calcium sensitivity of the fluorescent NO indicator 4, 5-diaminofluorescein (DAF-2): implications for cellular NO imaging. FEBS Lett. 491:227-232. (Pubitemid 32193801)
104. Kojima H, Urano Y, Kikuchi K, Higuchi T, Hirata Y, Nagano T. 1999. Fluorescent indicators for imaging nitric oxide production. Angew. Chem. Int. Ed. Engl. 38:3209-212. (Pubitemid 29533899)
105. Kojima H, Hirotani M, Nakatsubo N, Kikuchi K, Urano Y, et al. 2001. Bioimaging of nitric oxide with fluorescent indicators based on the rhodamine chromophore. Anal. Chem. 73:1967-973. (Pubitemid 32862401)
106. Heiduschka P, Thanos S. 1998. NO production during neuronal cell death can be directly assessed by a chemical reaction in vivo. NeuroReport 9:4051-057. (Pubitemid 29030687)
107. Galindo F, Kabir N, Gavrilovic J, Russell DA. 2008. Spectroscopic studies of 1, 2-diaminoanthraquinone (DAQ) as a fluorescent probe for the imaging of nitric oxide in living cells. Photochem. Photobiol. Sci. 7:126-130.
108. Gabe Y, Ueno T, Urano Y, Kojima H, Nagano T. 2006. Tunable design strategy for fluorescence probes based on 4-substituted BODIPY chromophore: improvement of highly sensitive fluorescence probe for nitric oxide. Anal. Bioanal. Chem. 386:621-626. (Pubitemid 44450942)
109. Gabe Y, Urano Y, Kikuchi K, Kojima H, Nagano T. 2004. Highly sensitive fluorescence probes for nitric oxide based on boron dipyrromethene chromophore-rational design of potentially useful bioimaging fluorescence probe. J. Am. Chem. Soc. 126:3357-367. (Pubitemid 38380736)
110. Sasaki E, Kojima H, Nishimatsu H, Urano Y, Kikuchi K, et al. 2005. Highly sensitive near-infrared fluorescent probes for nitric oxide and their application to isolated organs. J. Am. Chem. Soc. 127:3684-85. (Pubitemid 40411394)
111. Izumi S, Urano Y, Hanaoka K, Terai T, Nagano T. 2009. A simple and effective strategy to increase the sensitivity of fluorescence probes in living cells. J. Am. Chem. Soc. 131:10189-200.
112. Zhang R, Ye Z, Wang G, Zhang W, Yuan J. 2010. Development of a ruthenium(II) complex based luminescent probe for imaging nitric oxide production in living cells. Chem. Eur. J. 16:6884-891.
113. Kim JH, Heller DA, Jin H, Barone PW, Song C, et al. 2009. The rational design of nitric oxide selectivity in single-walled carbon nanotube near-infrared fluorescence sensors for biological detection. Nat. Chem. 1:473-481.
114. Yang Y, Seidlits SK, AdamsMM, LynchVM, Schmidt CE, et al. 2010. A highly selective low-background fluorescent imaging agent for nitric oxide. J. Am. Chem. Soc. 132:13114-116.
115. LimMH, Xu D, Lippard SJ. 2006. Visualization of nitric oxide in living cells by a copper-based fluorescent probe. Nat. Chem. Biol. 2:375-380. (Pubitemid 43936938)
116. Lim MH, Wong BA, Pitcock WH, Mokshagundam D, Baik MH, Lippard SJ. 2006. Direct nitric oxide detection in aqueous solution by copper(II) fluorescein complexes. J. Am. Chem. Soc. 128:14364-373. (Pubitemid 44707746)
117. Lim MH, Lippard SJ. 2007. Metal-based turn-on fluorescent probes for sensing nitric oxide. Acc. Chem. Res. 40:41-51.
118. McQuade LE, Pluth MD, Lippard SJ. 2010. Mechanism of nitric oxide reactivity and fluorescence enhancement of the NO-specific probe CuFL1. Inorg. Chem. 49:8025-033.
119. Gusarov I, Starodubtseva M, Wang ZQ, McQuade L, Lippard SJ, et al. 2008. Bacterial nitric-oxide synthases operate without a dedicated redox partner. J. Biol. Chem. 283:13140-147.
120. Shatalin K, Gusarov I, Avetissova E, Shatalina Y, McQuade LE, et al. 2008. Bacillus anthracis-derived nitric oxide is essential for pathogen virulence and survival in macrophages. Proc. Natl. Acad. Sci. USA 105:1009-013. (Pubitemid 351282072)
121. McQuade LE, Lippard SJ. 2010. Fluorescence-based nitric oxide sensing by Cu(II) complexes that can be trapped in living cells. Inorg. Chem. 49:7464-471.
122. McQuade LE, Ma J, Lowe G, Ghatpande A, Gelperin A, Lippard SJ. 2010. Visualization of nitric oxide production in the mouse main olfactory bulb by a cell-trappable copper(II) fluorescent probe. Proc. Natl. Acad. Sci. USA 107:8525-530.
123. Ouyang J, Hong H, Shen C, Zhao Y, OuyangCG, et al. 2008. A novel fluorescent probe for the detection of nitric oxide in vitro and in vivo. Free Radic. Biol. Med. 45:1426-436.
124. Ortiz M, Torŕens M, Mola JL, Ortiz PJ, Fragoso A, et al. 2008. Nitric oxide binding and photodelivery based on ruthenium(II) complexes of 4-arylazo-3, 5-dimethylpyrazole. Dalton Trans. (27):3559-566.
125. Soh N, Katayama Y, Maeda M. 2001. A fluorescent probe for monitoring nitric oxide production using a novel detection concept. Analyst 126:564-566. (Pubitemid 32453028)
126. Katayama Y, Takahashi S, Maeda M. 1998. Design, synthesis and characterization of a novel fluorescent probe for nitric oxide (nitrogen monoxide). Anal. Chim. Acta 365:159-167. (Pubitemid 28254746)
127. Lim MH, Lippard SJ. 2004. Fluorescence-based nitric oxide detection by ruthenium porphyrin fluorophore complexes. Inorg. Chem. 43:6366-370.
128. Hilderbrand SA, Lim MH, Lippard SJ. 2004. Dirhodium tetracarboxylate scaffolds as reversible fluorescence-based nitric oxide sensors. J. Am. Chem. Soc. 126:4972-978. (Pubitemid 38490164)
129. Eroy-Reveles AA, Mascharak PK. 2009. Nitric oxide-donating materials and their potential in pharmacological applications for site-specific nitric oxide delivery. Future Med. Chem. 1:1497-507.
130. Patra AK, Rose MJ, Murphy KA, Olmstead MM, Mascharak PK. 2004. Photolabile ruthenium nitrosyls with planar dicarboxamide tetradentate N4 ligands: effects of in-plane and axial ligand strength on NO release. Inorg. Chem. 43:4487-495.
131. Patra AK, Afshar R, Olmstead MM, Mascharak PK. 2002. The first non-heme iron(III) complex with a ligated carboxamido group that exhibits photolability of a bound NO ligand. Angew. Chem. Int. Ed. 41:2512-515. (Pubitemid 34803456)
132. Pearce LL, Gandley RE, Han WP, Wasserloos K, Stitt M, et al. 2000. Role of metallothionein in nitric oxide signaling as revealed by a green fluorescent fusion protein. Proc. Natl. Acad. Sci. USA 97:477-482. (Pubitemid 30055856)
133. Barker SLR, Clark HA, Swallen SF, Kopelman R, Tsang AW, Swanson JA. 1999. Ratiometric and fluorescence-lifetime-based biosensors incorporating cytochromec and the detection of extra- and intracellular macrophage nitric oxide. Anal. Chem. 71:1767-772. (Pubitemid 29222171)
134. Barker SLR, Zhao YD, Marletta MA, Kopelman R. 1999. Cellular applications of a sensitive and selective fiber-optic nitric oxide biosensor based on a dye-labeled heme domain of soluble guanylate cyclase. Anal. Chem. 71:2071-075.
135. Honda A, Adams SR, Sawyer CL, Lev-Ram V, Tsien RY, DostmannWRG. 2001. Spatiotemporal dynamics of guanosine 3′, 5′-cyclic monophosphate revealed by a genetically encoded, fluorescent indicator. Proc. Natl. Acad. Sci. USA 98:2437-442. (Pubitemid 32209500)
136. Sato M, Nakajima T, Goto M, Umezawa Y. 2006. Cell-based indicator to visualize picomolar dynamics of nitric oxide release from living cells. Anal. Chem. 78:8175-182. (Pubitemid 44927592)
137. Sato M, Hida N, Umezawa Y. 2005. Imaging the nanomolar range of nitric oxide with an amplifiercoupled fluorescent indicator in living cells. Proc. Natl. Acad. Sci. USA 102:14515-520. (Pubitemid 41457089)
138. Sato M, Hida N, Ozawa T, Umezawa Y. 2000. Fluorescent indicators for cyclic GMP based on cyclic GMP-dependent protein kinase Iαand green fluorescent proteins. Anal. Chem. 72:5918-924. (Pubitemid 32002666)
139. Cuajungco MP, Lees GJ. 1998. Nitric oxide generators produce accumulation of chelatable zinc in hippocampal neuronal perikarya. Brain Res. 799:118-129. (Pubitemid 28351211)
140. Bossy-Wetzel E, Talantova MV, LeeWD, ScholzkeMN, Harrop A, et al. 2004. Crosstalk between nitric oxide and zinc pathways to neuronal cell death involving mitochondrial dysfunction and p38-activated K+ channels. Neuron 41:351-365. (Pubitemid 38221040)
141. 2+ in cultured neurons after brief exposure to low concentrations of exogenous nitric oxide. BioMetals 20:891-901. (Pubitemid 350029531)
142. Kim YH, Koh JY. 2002. The role ofNADPH oxidase and neuronal nitric oxide synthase in zinc-induced poly(ADP-ribose) polymerase activation and cell death in cortical culture. Exp. Neurol. 177:407-418.
143. Berendji D, Kolb-Bachofen V, Meyer KL, Grapenthin O, Weber H, et al. 1997. Nitric oxide mediates intracytoplasmic and intranuclear zinc release. FEBS Lett. 405:37-41. (Pubitemid 27130368)
144. St Croix CM, Wasserloos KJ, Dineley KE, Reynolds IJ, Levitan ES, Pitt BR. 2002. Nitric oxide-induced changes in intracellular zinc homeostasis are mediated by metallothionein/thionein. Am. J. Physiol. Lung Cell. Mol. Physiol. 282:L185-192. (Pubitemid 34654669)
145. Tang Z-L, Wasserloos KJ, Liu XH, Stitt MS, Reynolds IJ, et al. 2002. Nitric oxide decreases the sensitivity of pulmonary endothelial cells to LPS-induced apoptosis in a zinc-dependent fashion. Mol. Cell. Biochem. 234:211-217. (Pubitemid 34777859)
146. 2+ resembles that of NO-mediated nitrosative stress, and is protected by MT-1 overexpression. Am. J. Physiol. Cell Physiol. 291:C555-568. (Pubitemid 44343639)
147. Bernal PJ, Leelavanichkul K, Bauer E, Cao R, Wilson A, et al. 2008. Nitric oxide-mediated zinc release contributes to hypoxic regulation of pulmonary vascular tone. Circ. Res. 102:1575-583.
148. 2+ via cGMP/PKG signaling pathway and prevents mitochondrial oxidant damage in cardiomyocytes. Cardiovasc. Res. 75:426-433. (Pubitemid 46961936)
149. Haase H, Rink L. 2009. Functional significance of zinc-related signaling pathways in immune cells. Annu. Rev. Nutr. 29:133-152.
150. Pautz A, Art J, Hahn S, Nowag S, Voss C, Kleinert H. 2010. Regulation of the expression of inducible nitric oxide synthase. Nitric Oxide 23:75-93.
151. Yamaoka J, Kume T, Akaike A, Miyachi Y. 2000. Suppressive effect of zinc ion on iNOS expression induced by interferon-γor tumor necrosis factor-αin murine keratinocytes. J. Dermatol. Sci. 23:27-35. (Pubitemid 30107837)
152. 2+ inhibits nitric oxide formation in response to lipopolysaccharides: implication in its anti-inflammatory activity. Eur. J. Pharmacol. 341:265-272. (Pubitemid 28131124)
153. 2+ release. Proc. Natl. Acad. Sci. USA 100:13952-957. (Pubitemid 37499172)
154. Kauppinen TM, Higashi Y, Suh SW, Escartin C, Nagasawa K, Swanson RA. 2008. Zinc triggers microglial activation. J. Neurosci. 28:5827-835.
155. Sensi SL, Ton-That D, Weiss JH, Rothe A, Gee KR. 2003. A new mitochondrial fluorescent zinc sensor. Cell Calcium 34:281-284. (Pubitemid 37009936)
156. 2+ pools. Proc. Natl. Acad. Sci. USA 100:6157-62 (Pubitemid 36576947)