Nitric oxide regulates neuronal activity via calcium-activated potassium channels

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Zhong, Lei Ray ^a   Estes, Stephen ^a   Artinian, Liana ^a   Rehder, Vincent ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4-AMINOPYRIDINE; ACTION POTENTIALS; ANIMALS; APAMIN; CALCIUM CHANNELS; CELLS, CULTURED; GANGLIA, AUTONOMIC; GROWTH CONES; HELIX (SNAILS); MOTOR NEURONS; NITRIC OXIDE; NITRIC OXIDE DONORS; PATCH-CLAMP TECHNIQUES; PEPTIDES; POTASSIUM CHANNEL BLOCKERS; POTASSIUM CHANNELS, CALCIUM-ACTIVATED; TETRAETHYLAMMONIUM;

EID: 84893521416     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0078727     Document Type: Article

References (51)

1. Bicker G (2007) Pharmacological approaches to nitric oxide signalling during neural development of locusts and other model insects. Arch Insect Biochem Physiol 64: 43-58.
2. Nikonenko I, Boda B, Steen S, Knott G, Welker E, et al. (2008) PSD-95 promotes synaptogenesis and multiinnervated spine formation through nitric oxide signaling. J Cell Biol 183: 1115-1127.
3. Hopper RA, Garthwaite J (2006) Tonic and phasic nitric oxide signals in hippocampal long-term potentiation. J Neurosci 26: 11513-11521. (Pubitemid 44772122)
4. Kemenes I, Kemenes G, Andrew RJ, Benjamin PR, O'Shea M (2002) Critical time-window for NO-cGMP-dependent long-term memory formation after one-trial appetitive conditioning. J Neurosci 22: 1414-1425. (Pubitemid 34163742)
5. Katzoff A, Ben-Gedalya T, Hurwitz I, Miller N, Susswein YZ, et al. (2006) Nitric oxide signals that aplysia have attempted to eat, a necessary component of memory formation after learning that food is inedible. J Neurophysiol 96: 1247-1257. (Pubitemid 44371518)
6. Garthwaite J (2008) Concepts of neural nitric oxide-mediated transmission. Eur J Neurosci 27: 2783-2802.
7. Tozer AJ, Forsythe ID, Steinert JR (2012) Nitric oxide signalling augments neuronal voltage-gated L-type (Ca(v)1) and P/q-type (Ca(v)2.1) channels in the mouse medial nucleus of the trapezoid body. PLoS ONE 7: e32256.
8. Steinert JR, Kopp-Scheinpflug C, Baker C, Challiss RA, Mistry R, et al. (2008) Nitric oxide is a volume transmitter regulating postsynaptic excitability at a glutamatergic synapse. Neuron 60: 642-656.
9. Wilson GW, Garthwaite J (2010) Hyperpolarization-activated ion channels as targets for nitric oxide signalling in deep cerebellar nuclei. Eur J Neurosci 31: 1935-1945.
10. Moroz LL, Kohn AB (2011) Parallel evolution of nitric oxide signaling: diversity of synthesis and memory pathways. Front Biosci 16: 2008-2051.
11. Van Wagenen S, Rehder V (1999) Regulation of neuronal growth cone filopodia by nitric oxide. J Neurobiol 39: 168-185. (Pubitemid 29190624)
12. 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. (Pubitemid 32105832)
13. Trimm KR, Rehder V (2004) Nitric oxide acts as a slow-down and search signal in developing neurites. Eur J Neurosci 19: 809-818. (Pubitemid 38297018)
14. Artinian L, Tornieri K, Zhong L, Baro D, Rehder V (2010) Nitric oxide acts as a volume transmitter to modulate electrical properties of spontaneously firing neurons via apamin-sensitive potassium channels. J Neurosci 30: 1699-1711.
15. Artinian L, Zhong L, Yang H, Rehder V (2012) Nitric oxide as intracellular modulator: internal production of NO increases neuronal excitability via modulation of several ionic conductances. Eur J Neurosci 36: 3333-3343.
16. Kemenes I, Straub VA, Nikitin ES, Staras K, O'Shea M, et al. (2006) Role of delayed nonsynaptic neuronal plasticity in long-term associative memory. Curr Biol 16: 1269-1279. (Pubitemid 43975371)
17. Lukowiak K, Martens K, Orr M, Parvez K, Rosenegger D, et al. (2006) Modulation of aerial respiratory behaviour in a pond snail. Respir Physiol Neurobiol 154: 61-72. (Pubitemid 44666573)
18. Susswein AJ, Chiel HJ (2012) Nitric oxide as a regulator of behavior: new ideas from Aplysia feeding. Prog Neurobiol 97: 304-317.
19. Miller N, Saada R, Fishman S, Hurwitz I, Susswein AJ (2011) Neurons controlling Aplysia feeding inhibit themselves by continuous NO production. PLoS ONE 6: e17779.
20. Miller N, Saada R, Markovich S, Hurwitz I, Susswein AJ (2011) L-arginine via nitric oxide is an inhibitory feedback modulator of Aplysia feeding. J Neurophysiol 105: 1642-1650.
21. Katzoff A, Ben-Gedalya T, Susswein AJ (2002) Nitric oxide is necessary for multiple memory processes after learning that a food is inedible in aplysia. J Neurosci 22: 9581-9594. (Pubitemid 35356200)
22. Kobayashi S, Ogawa H, Fujito Y, Ito E (2000) Nitric oxide suppresses fictive feeding response in Lymnaea stagnalis. Neurosci Lett 285: 209-212. (Pubitemid 30252065)
23. Moroz LL, Park JH, Winlow W (1993) Nitric oxide activates buccal motor patterns in Lymnaea stagnalis. Neuroreport 4: 643-646. (Pubitemid 23190881)
24. Elphick MR, Kemenes G, Staras K, O'Shea M (1995) Behavioral role for nitric oxide in chemosensory activation of feeding in a mollusc. J Neurosci 15: 7653-7664.
25. Quinlan EM, Arnett BC, Murphy AD (1997) Feeding stimulants activate an identified dopaminergic interneuron that induces the feeding motor program in Helisoma. J Neurophysiol 78: 812-824. (Pubitemid 27353546)
26. Murphy AD (2001) The neuronal basis of feeding in the snail, Helisoma, with comparisons to selected gastropods. Prog Neurobiol 63: 383-408.
27. Turner MB, Szabo-Maas TM, Poyer JC, Zoran MJ (2011) Regulation and restoration of motoneuronal synaptic transmission during neuromuscular regeneration in the pulmonate snail Helisoma trivolvis. Biol Bull 221: 110-125.
28. Sadamoto H, Hatakeyama D, Kojima S, Fujito Y, Ito E (1998) Histochemical study on the relation between NO-generative neurons and central circuitry for feeding in the pond snail, Lymnaea stagnalis. Neurosci Res 32: 57-63. (Pubitemid 28495579)
29. Zhong LR, Estes S, Artinian L, Rehder V (2013) Acetylcholine elongates neuronal growth cone filopodia via activation of nicotinic acetylcholine receptors. Dev Neurobiol 73: 487-501.
30. Zhong LR, Artinian L, Rehder V (2013) Dopamine suppresses neuronal activity of Helisoma B5 neurons via a D2-like receptor, activating PLC and K channels. Neuroscience 228: 109-119.
31. Hui K, Feng ZP (2008) NCS-1 differentially regulates growth cone and somata calcium channels in Lymnaea neurons. Eur J Neurosci 27: 631-643. (Pubitemid 351239285)
32. Welshhans K, Rehder V (2005) Local activation of the nitric oxide/cyclic guanosine monophosphate pathway in growth cones regulates filopodial length via protein kinase G, cyclic ADP ribose and intracellular Ca2+ release. Eur J Neurosci 22: 3006-3016. (Pubitemid 43001984)
33. Candia S, Garcia ML, Latorre R (1992) Mode of action of iberiotoxin, a potent blocker of the large conductance Ca(2+)-activated K+ channel. Biophys J 63: 583-590.
34. Alderton W, Cooper C, Knowles R (2001) Nitric oxide synthases: structure, function and inhibition. Biochem J 357: 593-615. (Pubitemid 32735142)
35. Torreano PJ, Cohan CS (1997) Electrically induced changes in Ca2+ in Helisoma neurons: regional and neuron-specific differences and implications for neurite outgrowth. J Neurobiol 32: 150-162. (Pubitemid 27057512)
36. Rehder V, Kater SB (1992) Regulation of neuronal growth cone filopodia by intracellular calcium. J Neurosci 12: 3175-3186.
37. Berridge MJ, Bootman MD, Roderick HL (2003) Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 4: 517-529. (Pubitemid 36773404)
38. Spitzer NC (2006) Electrical activity in early neuronal development. Nature 444: 707-712.
39. Mattson MP, Kater SB (1987) Calcium regulation of neurite elongation and growth cone motility. J Neurosci 7: 4034-4043. (Pubitemid 18012414)
40. Henley J, Poo MM (2004) Guiding neuronal growth cones using Ca2+ signals. Trends Cell Biol 14: 320-330. (Pubitemid 38798181)
41. Prast H, Philippu A (2001) Nitric oxide as modulator of neuronal function. Prog Neurobiol 64: 51-68. (Pubitemid 32201889)
42. Herrera GM, Nelson MT (2002) Differential regulation of SK and BK channels by Ca(2+) signals from Ca(2 +) channels and ryanodine receptors in guinea-pig urinary bladder myocytes. J Physiol 541: 483-492. (Pubitemid 35190214)
43. Cetiner M, Bennett MR (1993) Nitric oxide modulation of calcium-activated potassium channels in postganglionic neurones of avian cultured ciliary ganglia. Br J Pharmacol 110: 995-1002. (Pubitemid 24005231)
44. Bolotina VM, Najibi S, Palacino JJ, Pagano PJ, Cohen RA (1994) Nitric oxide directly activates calcium-dependent potassium channels in vascular smooth muscle. Nature 368: 850-853. (Pubitemid 24137748)
45. Schrofner S, Zsombok A, Hermann A, Kerschbaum HH (2004) Nitric oxide decreases a calcium-activated potassium current via activation of phosphodiesterase 2 in Helix U-cells. Brain Res 999: 98-105. (Pubitemid 38121455)
46. Tricoire L, Vitalis T (2012) Neuronal nitric oxide synthase expressing neurons: a journey from birth to neuronal circuits. Front Neural Circuits 6: 82.
47. Steinert JR, Robinson SW, Tong H, Haustein MD, Kopp-Scheinpflug C, et al. (2011) Nitric oxide is an activity-dependent regulator of target neuron intrinsic excitability. Neuron 71: 291-305.
48. Bean BP (2007) The action potential in mammalian central neurons. Nat Rev Neurosci 8: 451-465.
49. Park JH, Straub VA, O'Shea M (1998) Anterograde signaling by nitric oxide: characterization and in vitro reconstitution of an identified nitrergic synapse. J Neurosci 18: 5463-5476. (Pubitemid 28311961)
50. Moroz LL (2000) Giant identified NO-releasing neurons and comparative histochemistry of putative nitrergic systems in gastropod molluscs. Microsc Res Tech 49: 557-569.
51. Straub VA, Grant J, O'Shea M, Benjamin PR (2007) Modulation of serotonergic neurotransmission by nitric oxide. J Neurophysiol 97: 1088-1099. (Pubitemid 46239490)