The nitric oxide- cGMP signaling pathway differentially regulates presynaptic structural plasticity in cone and rod cells

Journal of Neuroscience

Volumn 25, Issue 10, 2005, Pages 2761-2770

  Zhang, Nan ^a   Beuve, Annie ^a   Townes Anderson, Ellen ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

cGMP; Cone; Neurite and varicosity formation; Neuritic sprouting; Nitric oxide; Rod; Soluble guanylyl cyclase

Indexed keywords

CALCIUM; CALCIUM CHANNEL L TYPE; CYCLIC GMP; CYCLIC GMP DEPENDENT PROTEIN KINASE; GUANYLATE CYCLASE; NITRIC OXIDE;

ANALYSIS OF VARIANCE; ARTICLE; CALCIUM TRANSPORT; DEVELOPMENT; ENZYME PHOSPHORYLATION; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NONHUMAN; PHOTORECEPTOR; PRESYNAPTIC NERVE; PRIORITY JOURNAL; RETINA CONE; RETINA ROD; SIGNAL TRANSDUCTION; STIMULATION; WESTERN BLOTTING;

AMBYSTOMA; ANIMALS; CELLS, CULTURED; CONES (RETINA); CYCLIC GMP; ENZYME INHIBITORS; NEURONAL PLASTICITY; NITRIC OXIDE; NITRIC OXIDE DONORS; PRESYNAPTIC TERMINALS; RODS (RETINA); SIGNAL TRANSDUCTION;

EID: 14944349039     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3195-04.2005     Document Type: Article

References (72)

1. Aggarwal BB, Mehta K (1996) Determination and regulation of nitric oxide production from macrophages by lipopolysaccharides, cytokines, and retinoids. Methods Enzymol 269:166-171.
2. Ahmad I, Barnstable CJ (1993) Differential laminar expression of particulate and soluble guanylate cyclase genes in rat retina. Exp Eye Res 56:51-62.
3. Aquirre G, Farber D, Lolley R, Fletcher RT, Chader GJ (1978) Rod-cone dysplasia in Irish setters: a defect in cyclic GMP metabolism in visual cells. Science 22:1133-1134.
4. Banin E, Cideciyan AV, Aleman TS, Petters RM, Wong F, Milam AH, Jacobson SG (1999) Retinal rod photoreceptor-specific gene mutation perturbs cone pathway development. Neuron 23:549-557.
5. Beavo JA (1995) Cyclic nucleotide phosphodiesterases: functional implications of multiple isoforms. Physiol Rev 75:725-748.
6. Blanks JC, Adinolfi AM, Lolley RN (1974) Photoreceptor degeneration and synaptogenesis in retinal-degenerative (rd) mice. J Comp Neurol 156:95-106.
7. Boer R, Ulrich W-R, Klein T, Mirau B, Haas S, Baur I (2000) The inhibitory potency and selectivity of arginine substrate site nitric-oxide synthase inhibitors is solely determined by their affinity toward the different isoenzymes. Mol Pharmacol 58:1026-1034.
8. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254.
9. Butt E, Eigenthaler M, Genieser HG (1994) (Rp)-8-pCPT-cGMPS, a novel cGMP-dependent protein kinase inhibitor. Eur J Pharmacol 269:265-268.
10. Cheung WS, Bhan I, Lipton SA (2000) Nitric oxide (NO.) stabilizes whereas nitrosonium (NO+) enhances filopodial outgrowth by rat retinal ganglion cells in vitro. Brain Res 868:1-13.
11. Cooper N, Liu L, Yoshida A, Pozdnyakov N, Margulis A, Sitaramayya A (1995) The bovine rod outer segment guanylate cyclase, ROS-GC, is present in both outer segment and synaptic layers of the retina. J Mol Neurosci 6:211-222.
12. Cuenca N, Lopez S, Howes K, Kolb H (1998) The localization of guanylyl cyclase-activating proteins in the mammalian retina. Invest Ophthalmol Vis Sci 39:1243-1250.
13. Domino SE, Tubb DJ, Garbers DL (1991) Assay of guanylyl cyclase catalytic activity. Methods Enzymol 195:345-355.
14. Farber DB, Lolley RN (1974) Cyclic guanosine monophosphate: elevation in degenerating photoreceptor cells of the C3H mouse retina. Science 186:449-451.
15. Fei Y (2002) Cone neurite sprouting: an early onset abnormality of the cone photoreceptors in the retinal degeneration mouse. Mol Vis 8:306-314.
16. Fisher SK, Lewis GP (2003) Muller cell and neuronal remodeling in retinal detachment and reattachment and their potential consequences for visual recovery: a review and reconsideration of recent data. Vision Res 43:887-897.
17. Friebe A, Koesling D (1998) Mechanism of YC-1-induced activation of soluble guanylyl cyclase. Mol Pharmacol 53:123-127.
18. Gamm DM, Barthel LK, Raymond PA, Uhler MD (2000) Localization of cGMP-dependent protein kinase isoforms in mouse eye. Invest Ophthalmol Vis Sci 41:2766-2773.
19. Gao YQ, Danciger M, Longmuir R, Piriev NI, Zhao DY, Heckenlively JR, Fishman GA, Weleber RG, Jacobson SG, Stone EM, Farber DB (1999) Screening of the gene encoding the α'-subunit of cone cGMP-PDE in patients with retinal degenerations. Invest Ophthalmol Vis Sci 40:1818-1822.
20. Garthwaite J (1995) Neural nitric oxide signalling. Trends Neurosci 18:51-52.
21. Garthwaite J, Southam E, Boulton CL, Nielsen EB, Schmidt K, Mayer B (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.
22. Haberecht MF, Schmidt HH, Mills SL, Massey SC, Nakane M, Redbum-Johnson DA (1998) Localization of nitric oxide synthase, NADPH diaphorase and soluble guanylyl cyclase in adult rabbit retina. Vis Neurosci 15:881-890.
23. Hicks D, Molday RS (1986) Differential immunogold-dextran labeling of bovine and frog rod and cone cells using monoclonal antibodies against bovine rhodopsin. Exp Eye Res 42:55-71.
24. Hobbs AJ (1997) Soluble guanylate cyclase: the forgotten sibling. Trends Pharmacol Sci 18:484-491.
25. Holscher C (1997) Nitric oxide, the enigmatic neuronal messenger: its role in synaptic plasticity. Trends Neurosci 20:298-303.
26. Ikeda S, Oka J, Nagao T (1991) Effects of four diltiazem stereoisomers on binding of D-cis-[3H]diltiazem and (+)-[3H]PN200-I10 to rabbit T-tubule calcium channels. Eur J Pharmacol 208:199-205.
27. Jägle H, Jägle C, Sérey L, Yu A, Rilk A, Sadowski B, Besch D, Zrenner E, Sharpe LT (2004) Visual short-term effects of Viagra: double-blind study in healthy young subjects. Am J Ophthalmol 137:842-849.
28. Ko FN, Wu CC, Kuo SC, Lee FY, Teng CM (1994) YC-1, a novel activator of platelet guanylate cyclase. Blood 84:4226-4233.
29. Kourennyi DE, Liu X, Hart J, Mahmud F, Baldridge WH, Barnes S (2004) Reciprocal modulation of calcium dynamics at rod and cone photoreceptor synapses by nitric oxide. J Neurophysiol 92:477-483.
30. Krizaj D, Lai FA, Copenhagen DR (2003) Ryanodine stores and calcium regulation in the inner segments of salamander rods and cones. J Physiol (Lond) 547:761-774.
31. Kurenny DE, Moroz LL, Turner RW, Sharkey KA, Barnes S (1994) Modulation of ion channels in rod photoreceptors by nitric oxide. Neuron 13:315-324.
32. Lamothe M, Chang FJ, Balashova N, Shirokov R, Beuve A (2004) Functional characterization of nitric oxide and YC-1 activation of soluble guanylyl cyclase: structural implication for the YC-1 binding site? Biochemistry 43:3039-3048.
33. Li ZY, Kljavin IJ, Milam AH (1995) Rod photoreceptor neurite sprouting in retinitis pigmentosa. J Neurosci 15:5429-5438.
34. Liepe BA, Stone C, Koistinaho J, Copenhagen DR (1994) Nitric oxide synthase in Müller cells and neurons of salamander and fish retina. J Neurosci 14:7641-7654.
35. Lipton SA, Choi YB, Pan ZH, Lei SZ, Chen HS, Sucher NJ, Loscalzo J, Singel DJ, Stamler JS (1993) A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds. Nature 364:626-632.
36. Liu X, Kourennyi DE (2004) D-S-nitrosocysteine inhibits the calcium channels in rod photoreceptors. Paper presented at Annual Meeting of Association for Research in Vision and Ophthalmology.
37. Liu X, Seno K, Nishizawa Y, Hayashi F, Yamazaki A, Matsumoto H, Wakabayashi T, Usukura J (1994) Ultrastructural localization of retinal guanylate cyclase in human and monkey retinas. Exp Eye Res 59:761-768.
38. MacLeish PR, Townes-Anderson E (1988) Growth and synapse formation among major classes of adult salamander retinal neurons in vitro. Neuron 1:751-760.
39. MacLeish PR, Barnstable CJ, Townes-Anderson E (1983) Use of a monoclonal antibody as a substrate for mature neurons in vitro. Proc Natl Acad Sci USA 80:7014-7018.
40. Mandell JW, MacLeish PR, Townes-Anderson E (1993) Process outgrowth and synaptic varicosity formation by adult photoreceptors in vitro. J Neurosci 13:3533-3548.
41. Marc RE, Jones BW, Watt CB, Strettoi E (2003) Neural remodeling in retinal degeneration. Prog Retin Eye Res 22:607-655.
42. Margulis A, Sitaramayya A (2000) Rate of deactivation of nitric oxide-stimulated soluble guanylate cyclase: influence of nitric oxide scavengers and calcium. Biochemistry 39:1034-1039.
43. Miller MJ, Thompson JH, Liu X, Eloby-Childress S, Sadowska-Krowicka H, Zhang XJ, Clark DA (1996) Failure of L-NAME to cause inhibition of nitric oxide synthesis: role of inducible nitric oxide synthase. Inflamm Res 45:272-276.
44. Morgans CW (1999) Calcium channel heterogeneity among cone photoreceptors in the tree shrew retina. Eur J Neurosci 11:2989-2993.
45. Morgans CW (2001) Localization of the alpha(1F) calcium channel subunit in the rat retina. Invest Ophthalmol Vis Sci 42:2414-2418.
46. Morgans CW, El Far O, Berntson A, Wassle H, Taylor WR (1998) Calcium extrusion from mammalian photoreceptor terminals. J Neurosci 18:2467-2474.
47. Nachman-Clewner M, Townes-Anderson E (1996) Injury-induced remodelling and regeneration of the ribbon presynaptic terminal in vitro. J Neurocytol 25:597-613.
48. Nachman-Clewner M, St Jules R, Townes-Anderson E (1999) L-type calcium channels in the photoreceptor ribbon synapse: localization and role in plasticity. J Comp Neurol 415:1-16.
49. Nathan C (1992) Nitric oxide as a secretory product of mammalian cells. FASEB J 6:3051-3064.
50. 2+ channels sets the polarity of nerve growth-cone turning. Nature 423:990-995.
51. Pfeifer A, Ruth P, Dostmann W, Sausbier M, Klatt P, Hofmann F (1999) Structure and function of cGMP-dependent protein kinases. Rev Physiol Biochem Pharmacol 135:105-149.
52. Polleux F, Morrow T, Ghosh A (2000) Semaphorin 3A is a chemoattractant for cortical apical dendrites. Nature 404:567-573.
53. Pugh Jr EN, Duda T, Sitaramayya A, Sharma RK (1997) Photoreceptor guanylate cyclases: a review. Biosci Rep 17:429-473.
54. Raviola E, Gilula NB (1973) Gap junctions between photoreceptor cells in the vertebrate retina. Proc Natl Acad Sci USA 70:1677-1681.
55. Rieke F, Schwartz EA (1994) A cGMP-gated current can control exocytosis at cone synapses. Neuron 13:863-873.
56. Savchenko A, Barnes S, Kramer RH (1997) Cyclic-nucleotide-gated channels mediate synaptic feedback by nitric oxide. Nature 390:694-698.
57. Schmidt H, Werner M, Heppenstall PA, Henning M, More MI, Kuhbandner S, Lewin GR, Hofmann F, Feil R, Rathjen FG (2002) cGMP-mediated signaling via cGKIalpha is required for the guidance and connectivity of sensory axons. J Cell Biol 159:489-498.
58. Sennlaub F, Courtois Y, Goureau O (2002) Inducible nitric oxide synthase mediates retinal apoptosis in ischemic proliferative retinopathy. J Neurosci 22:3987-3993.
59. Sherry DM, St Jules RS, Townes-Anderson E (1996) Morphologic and neurochemical target selectivity of regenerating adult photoreceptors in vitro. J Comp Neurol 376:476-488.
60. Sherry DM, Bui DD, Degrip WJ (1998) Identification and distribution of photoreceptor subtypes in the neotenic tiger salamander retina. Vis Neurosci 15:1175-1187.
61. Shimizu-Albergine M, Rybalkin SD, Rybalkina IG, Feil R, Wolfsgruber W, Hofmann F, Beavo JA (2003) Individual cerebellar Purkinje cells express different cGMP phosphodiesterases (PDEs): in vivo phosphorylation of cGMP-specific PDE (PDE5) as an indicator of cGMP-dependent protein kinase (PKG) activation. J Neurosci 23:6452-6459.
62. Song H, Ming G, He Z, Lehmann M, McKerracher L, Tessier-Lavigne M, Poo M (1998) Conversion of neuronal growth cone responses from repulsion to attraction by cyclic nucleotides. Science 281:1515-1518.
63. Townes-Anderson E, Chawla R, Zhang N (2003) Differential role of cAMP and cGMP in presynaptic plasticity of salamander cone and rod photoreceptors in vitro. Paper presented at Annual Meeting of Association for Research in Vision and Ophthalmology.
64. Trimm KR, Render V (2004) Nitric oxide acts as a slow-down and search signal in developing neurites. Eur J Neurosci 19:809-818.
65. Ueno S, Bambauer HJ, Umar H, Ueck M (1984) Localization and function of cyclic guanosine monophosphate-phosphodiesterase activity in the retinal rods of the rat by means of a newly developed cytochemical method. Cell Tissue Res 238:453-457.
66. Van Wagenen S, Rehder V (1999) Regulation of neuronal growth cone filopodia by nitric oxide. J Neurobiol 39:168-185.
67. Van Wagenen S, Rehder V (2001) Regulation of neuronal growth cone filopodia by nitric oxide depends on soluble guanylyl cyclase. J Neurobiol 46:206-219.
68. Wang X, Wang W, Li Y, Bai Y, Fiscus RR (1999) Mechanism of SNAP potentiating antiproliferative effect of calcitonin gene-related peptide in cultured vascular smooth muscle cells. J Mol Cell Cardiol 31:1599-1606.
69. Xiang Y, Li Y, Zhang Z, Cui K, Wang S, Yuan XB, Wu CP, Poo MM, Duan S (2002) Nerve growth cone guidance mediated by G protein-coupled receptors. Nat Neurosci 5:843-848.
70. Yun HY, Dawson VL, Dawson TM (1996) Neurobiology of nitric oxide. Crit Rev Neurobiol 10:291-316.
71. Zhang N, Townes-Anderson E (2002) Regulation of structural plasticity by different channel types in rod and cone photoreceptors. J Neurosci 22:7065-7079.
72. Zhuo M, Hu Y, Schultz C, Kandel ER, Hawkins RD (1994) Role of guanylyl cyclase and cGMP-dependent protein kinase in long-term potentiation. Nature 368:635-639.