Illuminating Cyclic Nucleotides: Sensors for cAMP and cGMP and Their Application in Live Cell Imaging (original) (raw)

• Rall TW et al (1957) The relationship of epinephrine and glucagon to liver phosphorylase Iv. Effect of epinephrine and glucagon on the reactivation of phosphorylase in liver homogenates. J Biol Chem 224:463–475
  Google Scholar
• Cook WH et al (1957) The formation of a cyclic dianhydrodiadenylic acid (I) by the alkaline degradation of adenosine-5′-triphosphoric acid (II) 1. J Am Chem Soc 79:3607–3608
  Article Google Scholar
• Lipkin D et al (1959) Adenosine-3′: 5′-phosphoric acid: a proof of structure1. J Am Chem Soc 81:6198–6203
  Article Google Scholar
• Sutherland EW, Rall TW (1957) The properties of an adenine ribonucleotide produced with cellular particles, ATP, Mg++, and epinephrine or glucagon. J Am Chem Soc 79:3608
  Article Google Scholar
• Makman RS, Sutherland EW (1965) Adenosine 3′,5′-phosphate in Escherichia coli. J Biol Chem 240:1309–1314
  Google Scholar
• Okabayashi T et al (1963) Occurrence of nucleotides in culture fluids of microorganisms V. Excretion of adenosine cyclic 3′,5′-Phosphate by Brevibacterium liquefaciens sp. n. J Bacteriol 86:930–936
  Google Scholar
• Ashman DF et al (1963) Isolation of adenosine 3′,5′-monophosphate and guanosine 3′,5′-monophosphate from rat urine. Biochem Biophys Res Commun 11:330–334
  Article Google Scholar
• Miki N et al (1975) Purification and properties of the light-activated cyclic nucleotide phosphodiesterase of rod outer segments. J Biol Chem 250:6320–6327
  Google Scholar
• Seifert R et al (2011) Cyclic CMP and cyclic UMP: new (old) second messengers. BMC Pharmacol 11:O34
  Article Google Scholar
• Ross P et al (1987) Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid. Nature 325:279–281
  Article Google Scholar
• Witte G et al (2008) Structural biochemistry of a bacterial checkpoint protein reveals diadenylate cyclase activity regulated by DNA recombination intermediates. Mol Cell 30:167–178
  Article Google Scholar
• Wu J et al (2013) Cyclic GMP-AMP is an endogenous second messenger in innate immune signaling by cytosolic DNA. Science 339:826–830
  Article Google Scholar
• Beavo JA, Brunton LL (2002) Cyclic nucleotide research—still expanding after half a century. Nat Rev Mol Cell Biol 3:710–718
  Article Google Scholar
• Beavo JA et al (1970) Hydrolysis of cyclic guanosine and adenosine 3′,5′-monophosphates by rat and bovine tissues. J Biol Chem 245:5649–5655
  Google Scholar
• Butcher RW, Sutherland EW (1962) Adenosine 3′,5′-phosphate in biological materials I. Purification and properties of cyclic 3′,5′-nucleotide phosphodiesterase and use of this enzyme to characterize adenosine 3′,5′-phosphate in human urine. J Biol Chem 237:1244–1250
  Google Scholar
• Hardman JG, Sutherland EW (1969) Guanyl cyclase, an enzyme catalyzing the formation of guanosine 3′,5′-monophosphate from guanosine triphosphate. J Biol Chem 244:6363–6370
  Google Scholar
• Sutherland EW et al (1962) Adenyl cyclase I. Distribution, preparation, and properties. J Biol Chem 237:1220–1227
  Google Scholar
• Lucas KA et al (2000) Guanylyl cyclases and signaling by cyclic GMP. Pharmacol Rev 52:375–414
  Google Scholar
• Steer ML (1975) Adenyl cyclase. Ann Surg 182:603–609
  Article Google Scholar
• Båhzu O, Danchin A (1994) Adenylyl cyclases: a heterogeneous class of ATP-utilizing enzymes, progress in nucleic acid research and molecular biology. Academic Press, Cambridge, Massachusetts, pp 241–283
  Google Scholar
• Danchin A (1993) Phylogeny of adenylyl cyclases. Adv Second Messenger Phosphoprot Res 27:109–162
  Google Scholar
• Shenoy AR et al (2002) The ascent of nucleotide cyclases: conservation and evolution of a theme. J Biosci 27:85–91
  Article Google Scholar
• Steegborn C (2014) Structure, mechanism, and regulation of soluble adenylyl cyclases—similarities and differences to transmembrane adenylyl cyclases. Biochimica et Biophysica Acta (BBA) (Molecular Basis of Disease) 1842:2535–2547
  Article Google Scholar
• Potter LR (2011) Guanylyl cyclase structure, function and regulation. Cell Signal 23:1921–1926
  Article Google Scholar
• Francis SH et al (2011) Mammalian cyclic nucleotide phosphodiesterases: molecular mechanisms and physiological functions. Physiol Rev 91:651–690
  Article Google Scholar
• Krebs EG et al (1959) Factors affecting the activity of muscle phosphorylase b kinase. J Biol Chem 234:2867–2873
  Google Scholar
• DeLange RJ et al (1968) Activation of skeletal muscle phosphorylase kinase by adenosine triphosphate and adenosine 3′,5′-monophosphate. J Biol Chem 243:2200–2208
  Google Scholar
• Walsh DA et al (1968) An adenosine 3′,5′-monophosphate-dependant protein kinase from rabbit skeletal muscle. J Biol Chem 243:3763–3765
  Google Scholar
• Kuo JF, Greengard P (1970) Cyclic nucleotide-dependent protein kinases VI. Isolation and partial purification of a protein kinase activated by guanosine 3′, 5′-monophosphate. J Biol Chem 245:2493–2498
  Google Scholar
• Kuo JF, Greengard P (1969) Cyclic nucleotide-dependent protein kinases, Iv. Widespread occurrence of adenosine 3′,5′-monophosphate-dependent protein kinase in various tissues and phyla of the Animal Kingdom. Proc Natl Acad Sci USA 64:1349–1355
  Article Google Scholar
• Sklar PB et al (1986) The odorant-sensitive adenylate cyclase of olfactory receptor cells. Differential stimulation by distinct classes of odorants. J Biol Chem 261:15538–15543
  Google Scholar
• Nakamura T, Gold GH (1987) A cyclic nucleotide-gated conductance in olfactory receptor cilia. Nature 325:442–444
  Article Google Scholar
• Robb RM (1974) Histochemical evidence of cyclic nucleotide phosphodiesterase in photoreceptor outer segments. Invest Ophthalmol Vis Sci 13:740–747
  Google Scholar
• Virmaux N et al (1976) Guanylate cyclase in vertebrate retina: evidence for specific association with rod outer segments. J Neurochem 26:233–235
  Article Google Scholar
• Goridis C, Virmaux N (1974) Light-regulated guanosine 3′, 5′-monophosphate phosphodiesterase of bovine retina. Nature 248:57–58
  Article Google Scholar
• Fesenko EE et al (1985) Induction by cyclic GMP of cationic conductance in plasma membrane of retinal rod outer segment. Nature 313:310–313
  Article Google Scholar
• Cook NJ et al (1987) Identification, purification, and functional reconstitution of the cyclic GMP-dependent channel from rod photoreceptors. Proc Natl Acad Sci USA 84:585–589
  Article Google Scholar
• Ludwig A et al (1998) A family of hyperpolarization-activated mammalian cation channels. Nature 393:587–591
  Article Google Scholar
• Kawasaki H et al (1998) A family of cAMP-binding proteins that directly activate Rap1. Science 282:2275–2279
  Article Google Scholar
• de Rooij J et al (1998) Epac is a Rap1 guanine-nucleotide-exchange factor directly activated by cyclic AMP. Nature 396:474–477
  Article Google Scholar
• Nambi S et al (2010) cAMP-regulated protein lysine acetylases in mycobacteria. J Biol Chem 285:24313–24323
  Article Google Scholar
• Endoh T, Engel JN (2009) CbpA: a polarly localized novel cyclic AMP-binding protein in Pseudomonas aeruginosa. J Bacteriol 191:7193–7205
  Article Google Scholar
• Charbonneau H et al (1990) Identification of a noncatalytic cGMP-binding domain conserved in both the cGMP-stimulated and photoreceptor cyclic nucleotide phosphodiesterases. Proc Natl Acad Sci USA 87:288–292
  Article Google Scholar
• Aravind L, Ponting CP (1997) The GAF domain: an evolutionary link between diverse phototransducing proteins. Trends Biochem Sci 22:458–459
  Article Google Scholar
• Martins TJ et al (1982) Purification and characterization of a cyclic GMP-stimulated cyclic nucleotide phosphodiesterase from bovine tissues. J Biol Chem 257:1973–1979
  Google Scholar
• Mumby MC et al (1982) Identification of cGMP-stimulated cyclic nucleotide phosphodiesterase in lung tissue with monoclonal antibodies. J Biol Chem 257:13283–13290
  Google Scholar
• Korsa I, Böck A (1997) Characterization of fhlA mutations resulting in ligand-independent transcriptional activation and ATP hydrolysis. J Bacteriol 179:41–45
  Article Google Scholar
• Anantharaman V et al (2001) Regulatory potential, phyletic distribution and evolution of ancient, intracellular small-molecule-binding domains1. J Mol Biol 307:1271–1292
  Article Google Scholar
• Zoraghi R et al (2004) Properties and functions of GAF domains in cyclic nucleotide phosphodiesterases and other proteins. Mol Pharmacol 65:267–278
  Article Google Scholar
• Martinez SE et al (2002) GAF domains: two-billion-year-old molecular switches that bind cyclic nucleotides. Mol Interv 2:317–323
  Article Google Scholar
• McKay DB, Steitz TA (1981) Structure of catabolite gene activator protein at 2.9 |[angst]| resolution suggests binding to left-handed B-DNA. Nature 290:744–749
  Article Google Scholar
• McKay DB et al (1982) Structure of catabolite gene activator protein at 2.9-A resolution. Incorporation of amino acid sequence and interactions with cyclic AMP. J Biol Chem 257:9518–9524
  Google Scholar
• Takio K et al (1982) Primary structure of the regulatory subunit of type II cAMP-dependent protein kinase from bovine cardiac muscle. Proc Natl Acad Sci 79:2544–2548
  Article Google Scholar
• Titani K et al (1984) Amino acid sequence of the regulatory subunit of bovine type I adenosine cyclic 3′,5′-phosphate dependent protein kinase. Biochemistry 23:4193–4199
  Article Google Scholar
• Takio K et al (1984) cGMP-dependent protein kinase, a chimeric protein homologous with two separate protein families. Biochemistry 23:4207–4218
  Article Google Scholar
• Canaves JM, Taylor SS (2002) Classification and phylogenetic analysis of the cAMP-dependent protein kinase regulatory subunit family. J Mol Evol 54:17–29
  Article Google Scholar
• Berman HM et al (2005) The cAMP binding domain: an ancient signaling module. Proc Natl Acad Sci USA 102:45–50
  Article Google Scholar
• Kannan N et al (2007) Evolution of allostery in the cyclic nucleotide binding module. Genome Biol 8:R264-1–R264-13
  Article Google Scholar
• Shabb JB, Corbin JD (1992) Cyclic nucleotide-binding domains in proteins having diverse functions. J Biol Chem 267:5723–5726
  Google Scholar
• Passner JM, Steitz TA (1997) The structure of a CAP-DNA complex having two cAMP molecules bound to each monomer. Proc Natl Acad Sci USA 94:2843–2847
  Article Google Scholar
• Mohanty S et al (2015) Structural and evolutionary divergence of cyclic nucleotide binding domains in eukaryotic pathogens: implications for drug design. Biochimica et Biophysica Acta (BBA) (Proteins and Proteomics) 1854:1575–1585
  Article Google Scholar
• Rehmann H et al (2007) Capturing cyclic nucleotides in action: snapshots from crystallographic studies. Nat Rev Mol Cell Biol 8:63–73
  Article Google Scholar
• Coccetti P et al (1995) The minimal active domain of the mouse Ras exchange factor CDC25Mm. Biochem Biophys Res Commun 206:253–259
  Article Google Scholar
• Gloerich M, Bos JL (2010) Epac: defining a new mechanism for cAMP action. Annu Rev Pharmacol Toxicol 50:355–375
  Article Google Scholar
• Builder SE et al (1980) The mechanism of activation of bovine skeletal-muscle protein-kinase by adenosine 3′-5′-monophosphate. J Biol Chem 255:3514–3519
  Google Scholar
• Francis SH, Corbin JD (1994) Structure and function of cyclic nucleotide-dependent protein kinases. Annu Rev Physiol 56:237–272
  Article Google Scholar
• Hofmann F et al (2000) Rising behind NO: cGMP-dependent protein kinases. J Cell Sci 113:1671–1676
  Google Scholar
• Hofmann F et al (2009) cGMP Regulated Protein Kinases (cGK), cGMP: generators, effectors and therapeutic implications. Springer, Berlin, pp 137–162
  Book Google Scholar
• Reed RB et al (1996) Fast and slow cyclic nucleotide-dissociation sites in camp-dependent protein kinase are transposed in type Iβ cGMP-dependent protein kinase. J Biol Chem 271:17570–17575
  Article Google Scholar
• Corbin JD et al (1986) Studies of Cgmp analog specificity and function of the 2 intrasubunit binding-sites of Cgmp-dependent protein-kinase. J Biol Chem 261:1208–1214
  Google Scholar
• Biel M, Michalakis S (2009) Cyclic Nucleotide-Gated Channels, cGMP: generators, effectors and therapeutic implications. Springer, Berlin, pp 111–136
  Book Google Scholar
• Biel M et al (2009) Hyperpolarization-activated cation channels: from genes to function. Physiol Rev 89:847–885
  Article Google Scholar
• Clayton GM et al (2004) Structural basis of ligand activation in a cyclic nucleotide regulated potassium channel. Cell 119:615–627
  Article Google Scholar
• Zagotta WN et al (2003) Structural basis for modulation and agonist specificity of HCN pacemaker channels. Nature 425:200–205
  Article Google Scholar
• Wainger BJ et al (2001) Molecular mechanism of cAMP modulation of HCN pacemaker channels. Nature 411:805–810
  Article Google Scholar
• Weber IT et al (1989) Predicted structures of the cGMP binding domains of the cGMP-dependent protein kinase: a key alanine/threonine difference in evolutionary divergence of cAMP and cGMP binding sites. Biochemistry 28:6122–6127
  Article Google Scholar
• Shabb JB et al (1990) One amino acid change produces a high affinity cGMP-binding site in cAMP-dependent protein kinase. J Biol Chem 265:16031–16034
  Google Scholar
• Altenhofen W et al (1991) Control of ligand specificity in cyclic nucleotide-gated channels from rod photoreceptors and olfactory epithelium. Proc Natl Acad Sci 88:9868–9872
  Article Google Scholar
• Varnum MD et al (1995) Molecular mechanism for ligand discrimination of cyclic nucleotide-gated channels. Neuron 15:619–625
  Article Google Scholar
• Kim JJ et al (2011) Co-crystal structures of PKG Iβ (92–227) with cGMP and cAMP Reveal the molecular details of cyclic-nucleotide binding. PLoS One 6:e18413
  Article Google Scholar
• Wall ME et al (2003) Mechanisms associated with cGMP binding and activation of cGMP-dependent protein kinase. Proc Natl Acad Sci USA 100:2380–2385
  Article Google Scholar
• Huang GY et al (2014) Structural basis for cyclic-nucleotide selectivity and cGMP-selective activation of PKG I. Structure 22:116–124
  Article Google Scholar
• Campbell JC et al (2016) Structural basis of cyclic nucleotide selectivity in cGMP-dependent protein kinase II. J Biol Chem 291:5623–5633
  Article Google Scholar
• McAllister-Lucas LM et al (1995) An essential aspartic acid at each of two allosteric cGMP-binding sites of a cGMP-specific phosphodiesterase. J Biol Chem 270:30671–30679
  Article Google Scholar
• Heikaus CC et al (2009) Cyclic nucleotide binding GAF domains from phosphodiesterases—structural and mechanistic insights. Structure 17:1551–1557
  Article Google Scholar
• Martinez SE et al (2002) The two GAF domains in phosphodiesterase 2A have distinct roles in dimerization and in cGMP binding. Proc Natl Acad Sci USA 99:13260–13265
  Article Google Scholar
• Pandit J et al (2009) Mechanism for the allosteric regulation of phosphodiesterase 2A deduced from the X-ray structure of a near full-length construct. Proc Natl Acad Sci USA 106:18225–18230
  Article Google Scholar
• Handa N et al (2008) Crystal structure of the GAF-B domain from human phosphodiesterase 10A complexed with its ligand, cAMP. J Biol Chem 283:19657–19664
  Article Google Scholar
• Heikaus CC et al (2008) Solution structure of the cGMP binding GAF domain from phosphodiesterase 5. J Biol Chem 283:22749–22759
  Article Google Scholar
• Martinez SE et al (2008) The structure of the GAF A domain from phosphodiesterase 6C reveals determinants of cGMP binding, a conserved binding surface, and a Large cGMP-dependent conformational change. J Biol Chem 283:25913–25919
  Article Google Scholar
• Wu AY et al (2004) Molecular determinants for cyclic nucleotide binding to the regulatory domains of phosphodiesterase 2A. J Biol Chem 279:37928–37938
  Article Google Scholar
• Manganiello VC et al (1995) Type-Iii Cgmp-Inhibited cyclic-nucleotide phosphodiesterases (Pde-3 Gene Family). Cell Signal 7:445–455
  Article Google Scholar
• Stangherlin A et al (2011) cGMP signals modulate cAMP Levels in a compartment-specific manner to regulate catecholamine-dependent signaling in cardiac myocytes novelty and significance. Circ Res 108:929–939
  Article Google Scholar
• Okada D, Asakawa S (2002) Allosteric activation of cGMP-Specific, cGMP-binding phosphodiesterase (PDE5) by cGMP. Biochemistry 41:9672–9679
  Article Google Scholar
• Rybalkina IG et al (2010) Multiple affinity states of cGMP-specific phosphodiesterase for sildenafil inhibition defined by cGMP-dependent and cGMP-independent mechanisms. Mol Pharmacol 77:670–677
  Article Google Scholar
• Biswas KH et al (2008) The GAF domain of the cGMP-binding, cGMP-specific phosphodiesterase (PDE5) is a sensor and a sink for cGMP. Biochemistry 47:3534–3543
  Article Google Scholar
• Hebert MC et al (1998) Structural features of the noncatalytic cGMP binding sites of frog photoreceptor phosphodiesterase using cGMP analogs. J Biol Chem 273:5557–5565
  Article Google Scholar
• Huang D et al (2004) Molecular determinants of cGMP binding to chicken cone photoreceptor phosphodiesterase. J Biol Chem 279:48143–48151
  Article Google Scholar
• Biswas KH et al (2015) Cyclic nucleotide binding and structural changes in the isolated GAF domain of Anabaena adenylyl cyclase, CyaB2. PeerJ 3:e882-1–e882-20
  Article Google Scholar
• Brooker G et al (1979) Radioimmunoassay of cyclic AMP and cyclic GMP. Adv Cycl Nucleotide Res 10:1–33
  Google Scholar
• Horton J, Baxendale P (1995) Mass measurements of cyclic AMP formation by radioimmunoassay, enzyme immunoassay, and scintillation proximity assay, signal transduction protocols. Humana Press, New York, pp 91–105
  Google Scholar
• Fagan KA et al (1999) Adenovirus-mediated Expression of an olfactory cyclic nucleotide-gated channel regulates the endogenous Ca2+-inhibitable adenylyl cyclase in C6-2B glioma cells. J Biol Chem 274:12445–12453
  Article Google Scholar
• Kramer RH (1990) Patch cramming: monitoring intracellular messengers in intact cells with membrane patches containing detector ion channels. Neuron 4:335–341
  Article Google Scholar
• Fagan KA et al (2001) Adenovirus encoded cyclic nucleotide-gated channels: a new methodology for monitoring cAMP in living cells. FEBS Lett 500:85–90
  Article Google Scholar
• Rich TC et al (2001) In vivo assessment of local phosphodiesterase activity using tailored cyclic nucleotide-gated channels as cAMP sensors. J Gen Physiol 118:63–78
  Article Google Scholar
• Visegrady A et al (2007) Application of the BD ACTOne technology for the high-throughput screening of Gs-coupled receptor antagonists. J Biomol Screen 12:1068–1073
  Article Google Scholar
• Trivedi B, Kramer RH (1998) Real-time patch-cram detection of intracellular cGMP reveals long-term suppression of responses to NO and muscarinic agonists. Neuron 21:895–906
  Article Google Scholar
• Rich TC et al (2000) Cyclic nucleotide-gated channels colocalize with adenylyl cyclase in regions of restricted cAMP diffusion. J Gen Physiol 116:147–161
  Article Google Scholar
• Willoughby D, Cooper DMF (2008) Live-cell imaging of cAMP dynamics. Nat Methods 5:29–36
  Article Google Scholar
• Paramonov VM et al (2015) Genetically-encoded tools for cAMP probing and modulation in living systems. Front Pharmacol 6:196-1–196-21
  Article Google Scholar
• Zadran S et al (2012) Fluorescence resonance energy transfer (FRET)-based biosensors: visualizing cellular dynamics and bioenergetics. Appl Microbiol Biot 96:895–902
  Article Google Scholar
• Adams SR et al (1991) Fluorescence ratio imaging of cyclic AMP in single cells. Nature 349:694–697
  Article Google Scholar
• Zaccolo M et al (2000) A genetically encoded, fluorescent indicator for cyclic AMP in living cells. Nat Cell Biol 2:25–29
  Article Google Scholar
• Ponsioen B et al (2004) Detecting cAMP-induced Epac activation by fluorescence resonance energy transfer: Epac as a novel cAMP indicator. EMBO Rep 5:1176–1180
  Article Google Scholar
• Nikolaev VO (2004) Novel single chain cAMP sensors for receptor-induced signal propagation. J Biol Chem 279:37215–37218
  Article Google Scholar
• Sprenger J, Nikolaev V (2013) Biophysical techniques for detection of cAMP and cGMP in living cells. Int J Mol Sci 14:8025–8046
  Article Google Scholar
• Klarenbeek J et al (2015) Fourth-generation Epac-based FRET sensors for cAMP feature exceptional brightness, photostability and dynamic range: characterization of dedicated sensors for FLIM, for ratiometry and with high affinity. PLoS One 10(4):e0122513-1–e0122513-11
  Google Scholar
• Nikolaev VO et al (2006) Cyclic AMP imaging in adult cardiac myocytes reveals far-reaching beta(1)-adrenergic but locally confined beta(2)-adrenergic receptor-mediated signaling. Circ Res 99:1084–1091
  Article Google Scholar
• Sato M et al (2000) Fluorescent indicators for cyclic GMP based on cyclic GMP-dependent protein kinase Iα and green fluorescent proteins. Anal Chem 72:5918–5924
  Article Google Scholar
• Honda A et al (2001) Spatiotemporal dynamics of guanosine 3′,5′-cyclic monophosphate revealed by a genetically encoded, fluorescent indicator. Proc Natl Acad Sci USA 98:2437–2442
  Article Google Scholar
• Nikolaev VO et al (2006) Fluorescent sensors for rapid monitoring of intracellular cGMP. Nat Methods 3:23–25
  Article Google Scholar
• Nausch LWM et al (2008) Differential patterning of cGMP in vascular smooth muscle cells revealed by single GFP-linked biosensors. Proc Natl Acad Sci USA 105:365–370
  Article Google Scholar
• Kitaguchi T et al (2013) Extracellular calcium influx activates adenylate cyclase 1 and potentiates insulin secretion in MIN6 cells. Biochem J 450:365–373
  Article Google Scholar
• Odaka H et al (2014) Genetically-encoded yellow fluorescent cAMP indicator with an expanded dynamic range for dual-color imaging. PLoS One 9:e100252
  Article Google Scholar
• Prinz A et al (2006) Novel, isotype-specific sensors for protein kinase A subunit interaction based on bioluminescence resonance energy transfer (BRET). Cell Signal 18:1616–1625
  Article Google Scholar
• Zaccolo M, Pozzan T (2002) Discrete microdomains with high concentration of cAMP in stimulated rat neonatal cardiac myocytes. Science 295:1711–1715
  Article Google Scholar
• Ostrom RS, Insel PA (2004) The evolving role of lipid rafts and caveolae in G protein-coupled receptor signaling: implications for molecular pharmacology. Br J Pharmacol 143:235–245
  Article Google Scholar
• Jiang LI et al (2007) Use of a cAMP BRET sensor to characterize a novel regulation of cAMP by the sphingosine 1-phosphate/G13 pathway. J Biol Chem 282:10576–10584
  Article Google Scholar
• Matthiesen K, Nielsen J (2011) Cyclic AMP control measured in two compartments in HEK293 cells: phosphodiesterase KM is more important than phosphodiesterase localization. PLoS One 6(9):e24392-1–e24392-8
  Article Google Scholar
• Barak LS et al (2008) Pharmacological characterization of membrane-expressed human trace amine-associated receptor 1 (TAAR1) by a bioluminescence resonance energy transfer cAMP biosensor. Mol Pharmacol 74:585–594
  Article Google Scholar
• Nambi S et al (2012) Cyclic AMP-induced conformational changes in mycobacterial protein acetyltransferases. J Biol Chem 287:18115–18129
  Article Google Scholar
• Modi S et al (2010) Structural DNA nanotechnology: from bases to bricks. From Structure to Function. J Phys Chem Lett 1:1994–2005
  Article Google Scholar
• Chakraborty K et al (2016) Nucleic acid-based nanodevices in biological imaging. Annu Rev Biochem 85:349–373
  Article Google Scholar
• Modi S et al (2009) A DNA nanomachine that maps spatial and temporal pH changes inside living cells. Nat Nanotechnol 4:325–330
  Article Google Scholar
• Surana S et al (2011) An autonomous DNA nanodevice captures pH maps of living cells in culture and in vivo. Lect Notes Comput Sci 6937:22–31
  Article Google Scholar
• Saha S et al (2015) A pH-independent DNA nanodevice for quantifying chloride transport in organelles of living cells. Nat Nanotechnol 10:645–652
  Article Google Scholar
• Ellington AD, Szostak JW (1990) Invitro selection of rna molecules that bind specific ligands. Nature 346:818–822
  Article Google Scholar
• Ellington AD, Szostak JW (1992) Selection in vitro of single-stranded DNA molecules that fold into specific ligand-binding structures. Nature 355:850–852
  Article Google Scholar
• Cho EJ et al (2009) Applications of aptamers as sensors. Annu Rev Anal Chem 2:241–264
  Article Google Scholar
• Paige JS et al (2011) RNA mimics of green fluorescent protein. Science 333:642–646
  Article Google Scholar
• Paige JS et al (2012) Fluorescence imaging of cellular metabolites with RNA. Science 335:1194
  Article Google Scholar
• Sharma S et al (2014) A fluorescent nucleic acid nanodevice quantitatively images elevated cyclic adenosine monophosphate in membrane-bound compartments. Small 10:4276–4280
  Article Google Scholar
• Zaccolo M (2009) cAMP signal transduction in the heart: understanding spatial control for the development of novel therapeutic strategies. Br J Pharmacol 158:50–60
  Article Google Scholar
• Tsai EJ, Kass DA (2009) Cyclic GMP signaling in cardiovascular pathophysiology and therapeutics. Pharmacol Ther 122:216–238
  Article Google Scholar
• Gorshkov K, Zhang J (2014) Visualization of cyclic nucleotide dynamics in neurons. Front Cell Neurosci 8:395-1–395-13
  Article Google Scholar
• Kleppisch T, Feil R (2009) cGMP signalling in the mammalian brain: role in synaptic plasticity and behaviour, cGMP: generators, effectors and therapeutic implications. Springer, Berlin, pp 549–579
  Book Google Scholar
• Froese A, Nikolaev VO (2015) Imaging alterations of cardiomyocyte cAMP microdomains in disease. Front Pharmacol 6:172-1–172-5
  Article Google Scholar
• Lomas O, Zaccolo M (2014) Phosphodiesterases maintain signaling fidelity via compartmentalization of cyclic nucleotides. Physiology 29:141–149
  Article Google Scholar
• Trivedi B, Kramer RH (2002) Patch cramming reveals the mechanism of long-term suppression of cyclic nucleotides in intact neurons. J Neurosci 22:8819–8826
  Google Scholar
• Shelly M et al (2010) Local and long-range reciprocal regulation of cAMP and cGMP in axon/dendrite formation. Science 327:547–552
  Article Google Scholar
• Puerto AD et al (2012) Adenylate cyclase 5 coordinates the action of ADP, P2Y1, P2Y13 and ATP-gated P2X7 receptors on axonal elongation. J Cell Sci 125:176–188
  Article Google Scholar
• Nicol X et al (2011) Spatial and temporal second messenger codes for growth cone turning. Proc Natl Acad Sci USA 108:13776–13781
  Article Google Scholar
• Castro LRV et al (2010) Type 4 phosphodiesterase plays different integrating roles in different cellular domains in pyramidal cortical neurons. J Neurosci 30:6143–6151
  Article Google Scholar
• Castro LRV et al (2013) Striatal neurones have a specific ability to respond to phasic dopamine release. J Physiol 591:3197–3214
  Article Google Scholar
• Polito M et al (2013) The NO/cGMP pathway inhibits transient cAMP signals through the activation of PDE2 in striatal neurons. Front Cell Neurosci 7:211-1–211-10
  Article Google Scholar
• Benedetto GD et al (2008) Protein kinase A type I and type II define distinct intracellular signaling compartments. Circ Res 103:836–844
  Article Google Scholar
• Dittrich M et al (2001) Local response of L-type Ca2+ current to nitric oxide in frog ventricular myocytes. J Physiol Lond 534:109–121
  Article Google Scholar
• Castro LRV et al (2006) Cyclic guanosine monophosphate compartmentation in rat cardiac myocytes. Circulation 113:2221–2228
  Article Google Scholar
• Castro LRV et al (2010) Feedback control through cGMP-dependent protein kinase contributes to differential regulation and compartmentation of cGMP in rat cardiac myocytes novelty and significance. Circ Res 107:1232–1240
  Article Google Scholar
• Bagorda A et al (2009) Real-time measurements of cAMP production in live Dictyostelium cells. J Cell Sci 122:3907–3914
  Article Google Scholar
• Gomes LC et al (2011) During autophagy mitochondria elongate, are spared from degradation and sustain cell viability. Nat Cell Biol 13:589–598
  Article Google Scholar
• Ferrandon S et al (2009) Sustained cyclic AMP production by parathyroid hormone receptor endocytosis. Nat Chem Biol 5:734–742
  Article Google Scholar
• Kotowski SJ et al (2011) Endocytosis promotes rapid dopaminergic signaling. Neuron 71:278–290
  Article Google Scholar
• Ballinger MN et al (2010) Transient increase in cyclic AMP localized to macrophage phagosomes. PLoS One 5(11):e13962-1–e13962-7
  Article Google Scholar
• Bloch A (1975) Uridine 3′,5′-monophosphate (cyclic UMP) I. Isolation from rat liver extracts. Biochem Biophys Res Commun 64:210–218
  Article Google Scholar
• Cech SY, Ignarro LJ (1977) Cytidine 3′,5′-monophosphate (cyclic CMP) formation in mammalian tissues. Science 198:1063–1065
  Article Google Scholar
• Hardman JG, Sutherland EW (1965) A cyclic 3′, 5′-nucleotide phosphodiesterase from heart with specificity for uridine 3′, 5′-phosphate. J Biol Chem 240:PC3704–PC3705
  Google Scholar
• Helfman DM et al (1981) Purification to homogeneity and general properties of a novel phosphodiesterase hydrolyzing cyclic CMP and cyclic AMP. J Biol Chem 256:6327–6334
  Google Scholar
• Newton RP et al (1984) Extraction, purification and identification of cytidine 3′,5′-cyclic monophosphate from rat tissues. Biochem J 221:665–673
  Article Google Scholar
• Römling U et al (2013) Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev 77:1–52
  Article Google Scholar
• Corrigan RM, Gründling A (2013) Cyclic di-AMP: another second messenger enters the fray. Nat Rev Microbiol 11:513–524
  Article Google Scholar
• Li X-D et al (2013) Pivotal roles of cGAS-cGAMP signaling in antiviral defense and immune adjuvant effects. Science 341:1390–1394
  Article Google Scholar
• Schaap P (2013) Cyclic di-nucleotide signaling enters the eukaryote domain. IUBMB Life 65:897–903
  Article Google Scholar
• Chen Z-H, Schaap P (2012) The prokaryote messenger c-di-GMP triggers stalk cell differentiation in Dictyostelium. Nature 488:680–683
  Article Google Scholar
• Banerjee A et al (2015) A universal stress protein (USP) in mycobacteria binds cAMP. J Biol Chem 290:12731–12743
  Article Google Scholar
• Serezani CH et al (2008) Cyclic AMP: master regulator of innate immune cell function. Am J Respir Cell Mol Biol 39:127–132
  Article Google Scholar
• McDonough KA, Rodriguez A (2011) The myriad roles of cyclic AMP in microbial pathogens: from signal to sword. Nat Rev Microbiol 10:27–38
  Google Scholar
• Arshad N, Visweswariah SS (2013) Cyclic nucleotide signaling in intestinal epithelia: getting to the gut of the matter. Wiley Interdiscip Rev Syst Biol Med 5:409–424
  Article Google Scholar
• Calebiro D, Maiellaro I (2014) cAMP signaling microdomains and their observation by optical methods. Front Cell Neurosci 8:350-1–350-9
  Article Google Scholar
• Götz KR et al (2014) Transgenic mice for real-time visualization of cGMP in intact adult cardiomyocytes. Circ Res 114:1235–1245
  Article Google Scholar
• Thunemann M et al (2013) Transgenic mice for cGMP imaging novelty and significance. Circ Res 113:365–371
  Article Google Scholar
• Koizumi M, Breaker RR (2000) Molecular recognition of cAMP by an RNA aptamer. Biochemistry 39:8983–8992
  Article Google Scholar
• Goulding EH et al (1994) Molecular mechanism of cyclic-nucleotide-gated channel activation. Nature 372:369–374
  Article Google Scholar
• Schultz SC et al (1991) Crystal-structure of a Cap-DNA Complex—the DNA Is Bent by 90-Degrees. Science 253:1001–1007
  Article Google Scholar
• The PyMOL Molecular Graphics System. Version 1.2r3pre, Schrödinger, LLC