Differential patterning of cGMP in vascular smooth muscle cells revealed by single GFP-linked biosensors

Proceedings of the National Academy of Sciences of the United States of America

Volumn 105, Issue 1, 2008, Pages 365-370

  Nausch, Lydia W M ^a   Ledoux, Jonathan ^a   Bonev, Adrian D ^a   Nelson, Mark T ^a   Dostmann, Wolfgang R ^a  

^a UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

Author keywords

cGMP dependent protein kinase; Confocal microscopy; Fluorescent biosensors; Natriuretic peptides; Nitric oxide

Indexed keywords

1H 1,2,4 OXADIAZOLO[4,3 A]QUINOXALIN 1 ONE; 8 BROMO CYCLIC GMP; ADENOVIRUS VECTOR; ATRIAL NATRIURETIC FACTOR; CYCLIC AMP; CYCLIC GMP; CYCLIC GMP DEPENDENT PROTEIN KINASE; FORSKOLIN; GREEN FLUORESCENT PROTEIN; NITRIC OXIDE; PHOSPHODIESTERASE V; PHOSPHODIESTERASE V INHIBITOR; PROTEIN KINASE G 1ALPHA; PROTEIN KINASE G 1BETA; SILDENAFIL; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; AORTA; ARTICLE; BIOSENSOR; CELL CULTURE; DISSOCIATION CONSTANT; ENZYME ACTIVITY; ENZYME INHIBITION; FLUORESCENCE; GENE DELETION; NONHUMAN; PRIORITY JOURNAL; RAT; SMOOTH MUSCLE FIBER; STATISTICAL SIGNIFICANCE; VASCULAR SMOOTH MUSCLE;

ANIMALS; AORTA; BIOSENSING TECHNIQUES; CALIBRATION; CYCLIC GMP; CYCLIC GMP-DEPENDENT PROTEIN KINASES; FLUORESCENCE RESONANCE ENERGY TRANSFER; GREEN FLUORESCENT PROTEINS; KINETICS; MICROSCOPY, CONFOCAL; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NATRIURETIC PEPTIDES; NITRIC OXIDE; RATS;

EID: 38349099574     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0710387105     Document Type: Article

References (47)

1. Conti M, Beavo J (2007) Biochemistry and physiology of cyclic nucleotide phosphodiesterases: Essential components in cyclic nucleotide signaling. Annu Rev Biochem 76:481-511.
2. Francis SH, Blount MA, Zoraghi R, Corbin JD (2005) Molecular properties of mammalian proteins that interact with cGMP: Protein kinases, cation channels, phosphodiesterases, and multi-drug anion transporters. Front Biosci 10:2097-2117.
3. Hofmann F, Biel M, Kaupp UB (2005) International Union of Pharmacology. LI. Nomenclature and structure-function relationships of cyclic nucleotide-regulated channels. Pharmacol Rev 57:455-462.
4. Hofmann F (2005) The biology of cyclic GMP-dependent protein kinases. J Biol Chem 280:1-4.
5. Kuhn M (2005) Cardiac and intestinal natriuretic peptides: Insights from genetically modified mice. Peptides 26:1078-1085.
6. Mullershausen F, Koesling D, Friebe A (2005) NO-sensitive guanylyl cyclase and NO-induced feedback inhibition in cGMP signaling. Front Biosci 10:1269-1278.
7. Garthwaite J (2005) Dynamics of cellular NO-cGMP signaling. Front Biosci 10:1868-1880.
8. Cary SP, Winger JA, Derbyshire ER, Marletta MA (2006) Nitric oxide signaling: No longer simply on or off. Trends Biochem Sci 31:231-239.
9. Honda A, Adams SR, Sawyer CL, Lev-Ram V, Tsien RY, Dostmann WR (2001) Spatiotemporal dynamics of guanosine 3′,5′-cyclic monophosphate revealed by a genetically encoded, fluorescent indicator. Proc Natl Acad Sci USA 98:2437-2442.
10. Nikolaev VO, Gambaryan S, Lohse MJ (2006) Fluorescent sensors for rapid monitoring of intracellular cGMP. Nat Methods 3:23-25.
11. Russwurm M, et al. (2007) Design of fluorescence resonance energy transfer (FRET)-based cGMP indicators: A systematic approach. Biochem J 407:69-77.
12. Cawley SM, Sawyer CL, Brunelle KF, van der Vliet A, Dostmann WR (2007) Nitric oxide-evoked transient kinetics of cyclic GMP in vascular smooth muscle cells. Cell Signal 19:1023-1033.
13. Honda A, Sawyer CL, Cawley SM, Dostmann WR (2005) Cygnets: In vivo characterization of novel cGMP indicators and in vivo imaging of intracellular cGMP. Methods Mol Biol 307:27-43.
14. Takimoto E, et al. (2005) cGMP catabolism by phosphodiesterase 5A regulates cardiac adrenergic stimulation by NOS3-dependent mechanism. Circ Res 96:100-109.
15. Mongillo M, et al. (2006) Compartmentalized phosphodiesterase-2 activity blunts beta-adrenergic cardiac inotropy via an NO/cGMP-dependent pathway. Circ Res 98:226-234.
16. Honda A, Moosmeier MA, Dostmann WR (2005) Membrane-permeable cygnets: Rapid cellular internalization of fluorescent cGMP-indicators. Front Biosci 10:1290-1301.
17. Mo E, Amin H, Bianco IH, Garthwaite J (2004) Kinetics of a cellular nitric oxide/cGMP/ phosphodiesterase-5 pathway. J Biol Chem 279:26149-26158.
18. Roy B, Garthwaite J (2006) Nitric oxide activation of guanylyl cyclase in cells revisited. Proc Natl Acad Sci USA 103:12185-12190.
19. Castro LR, Verde I, Cooper DM, Fischmeister R (2006) Cyclic guanosine monophosphate compartmentation in rat cardiac myocytes. Circulation 113:2221-2228.
20. Piggott LA, et al. (2006) Natriuretic peptides and nitric oxide stimulate cGMP synthesis in different cellular compartments. J Gen Physiol 128:3-14.
21. Takimoto E, et al. (2007) Compartmentalization of cardiac beta-adrenergic inotropy modulation by phosphodiesterase type 5. Circulation 115:2159-2167.
22. Fischmeister R, et al. (2006) Compartmentation of cyclic nucleotide signaling in the heart: The role of cyclic nucleotide phosphodiesterases. Circ Res 99:816-828.
23. Kass DA, Takimoto E, Nagayama T, Champion HC (2007) Phosphodiesterase regulation of nitric oxide signaling. Cardiovasc Res 75:303-314.
24. Baird GS, Zacharias DA, Tsien RY (1999) Circular permutation and receptor insertion within green fluorescent proteins. Proc Natl Acad Sci USA 96:11241-11246.
25. Nakai J, Ohkura M, Imoto K (2001) A high signal-to-noise Ca(2+) probe composed of a single green fluorescent protein. Nat Biotechnol 19:137-141.
26. 2+ indicator GCaMP2. Proc Natl Acad Sci USA 103:4753-4758.
27. Richie-Jannetta R, Busch JL, Higgins KA, Corbin JD, Francis SH (2006) Isolated regulatory domains of cGMP-dependent protein kinase I alpha and I beta retain dimerization and native cGMP-binding properties and undergo isoform-specific conformational changes. J Biol Chem 281:6977-6984.
28. 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.
29. Zhao J, et al. (1997) Progressive cyclic nucleotide-induced conformational changes in the cGMP-dependent protein kinase studied by small angle x-ray scattering in solution. J Biol Chem 272:31929-31936.
30. Ruth P, et al. (1991) The activation of expressed cGMP-dependent protein kinase isozymes I alpha and I beta is determined by the different amino-termini. Eur J Biochem 202:1339-1344.
31. Ruth P, et al. (1997) Identification of the amino acid sequences responsible for high affinity activation of cGMP kinase I alpha. J Biol Chem 272:10522-10528.
32. Wolfe L, Corbin JD, Francis SH (1989) Characterization of a novel isozyme of cGMP-dependent protein kinase from bovine aorta. J Biol Chem 264:7734-7741.
33. Dostmann WR, Koep N, Endres R (1996) The catalytic domain of the cGMP-dependent protein kinase I alpha modulates the cGMP-binding characteristics of its regulatory domain. FEBS Lett 398:206-210.
34. Griesbeck O, Baird GS, Campbell RE, Zacharias DA, Tsien RY (2001) Reducing the environmental sensitivity of yellow fluorescent protein: Mechanism and applications. J Biol Chem 276:29188-29194.
35. 2+ indicators with greatly improved fluorescence properties. J Biol Chem 260:3440-3450.
36. Zoraghi R, Bessay EP, Corbin JD, Francis SH (2005) Structural and functional features in human PDE5A1 regulatory domain that provide for allosteric cGMP binding, dimerization, and regulation. J Biol Chem 280:12051-12063.
37. Winquist RJ, Faison EP, Waldman SA, Schwartz K, Murad F, Rapoport RM (1984) Atrial natriuretic factor elicits an endothelium-independent relaxation and activates particulate guanylate cyclase in vascular smooth muscle. Proc Natl Acad Sci USA 81:7661-7664.
38. Leitman DC, et al. (1988) Atrial natriuretic peptide binding, cross-linking, and stimulation of cyclic GMP accumulation and particulate guanylate cyclase activity in cultured cells. J Biol Chem 263:3720-3728.
39. Hamet P, Pang SC, Tremblay J (1989) Atrial natriuretic factor-induced egression of cyclic guanosine 3′:5′-monophosphate in cultured vascular smooth muscle and endothelial cells. J Biol Chem 264:12364-12369.
40. Garthwaite J, et al. (1995) Potent and selective inhibition of nitric oxide-sensitive guanylyl cyclase by 1H-[1,2,4]oxadiazolo[4,3-a] quinoxalin-1-one. Mol Pharmacol 48:184-188.
41. Brunner F, Stessel H, Kukovetz WR (1995) Novel guanylyl cyclase inhibitor, ODQ reveals role of nitric oxide, but not of cyclic GMP in endothelin-1 secretion. FEBS Lett 376:262-266.
42. Schrammel A, Behrends S, Schmidt K, Koesling D, Mayer B (1996) Characterization of 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one as a heme-site inhibitor of nitric oxidesensitive guanylyl cyclase. Mol Pharmacol 50:1-5.
43. Turko IV, Ballard SA, Francis SH, Corbin JD (1999) Inhibition of cyclic GMP-binding cyclic GMP-specific phosphodiesterase (Type 5) by sildenafil and related compounds. Mol Pharmacol 56:124-130.
44. Corbin JD, et al. (2003) [3H]Sildenafil binding to phosphodiesterase-5 is specific, kinetically heterogeneous, and stimulated by cGMP. Mol Pharmacol 63:1364-1372.
45. Robertson BE, Schubert R, Hescheler J, Nelson MT (1993) cGMP-dependent protein kinase activates Ca-activated K channels in cerebral artery smooth muscle cells. Am J Physiol 265:C299-303.
46. 2+ sparks is involved in regulation of arterial diameter by cyclic nucleotides. Am J Physiol 274:C1346-C1355.
47. 2+-sensing transgenic mice: Postsynaptic signaling in smooth muscle. J Biol Chem 279:21461-21468.