Spinal nNOS regulates phrenic motor facilitation by a 5-HT2B receptor- and NADPH oxidase-dependent mechanism

Neuroscience

Volumn 269, Issue , 2014, Pages 67-78

  MacFarlane, P M ^a,b   Vinit, S ^a,c   Mitchell, G S ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b CASE WESTERN RESERVE UNIVERSITY   (United States)

^c LABORATOIRE DES SCIENCES DU CLIMAT ET DE L ENVIRONNEMENT   (France)

Author keywords

Intermittent hypoxia; Nitric oxide; Respiratory plasticity

Indexed keywords

CYCLIC GMP DEPENDENT PROTEIN KINASE; ENZYME INHIBITOR; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; NITRIC OXIDE DONOR; NOS1 PROTEIN, RAT; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SEROTONIN 2 ANTAGONIST; SEROTONIN 2B RECEPTOR; SUPEROXIDE DISMUTASE;

ACUTE DISEASE; ANIMAL; ANOXIA; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; MALE; METABOLISM; NERVE CELL PLASTICITY; PATHOPHYSIOLOGY; PHRENIC NERVE; PHYSIOLOGY; RAT; SPINAL CORD;

ACUTE DISEASE; ANIMALS; ANOXIA; CYCLIC GMP-DEPENDENT PROTEIN KINASES; ENZYME INHIBITORS; MALE; NADPH OXIDASE; NEURONAL PLASTICITY; NITRIC OXIDE; NITRIC OXIDE DONORS; NITRIC OXIDE SYNTHASE TYPE I; PHRENIC NERVE; RATS; REACTIVE OXYGEN SPECIES; RECEPTOR, SEROTONIN, 5-HT2B; SEROTONIN 5-HT2 RECEPTOR ANTAGONISTS; SPINAL CORD; SUPEROXIDE DISMUTASE;

EID: 84898611916     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2014.03.014     Document Type: Article

References (53)

1. Aley K.O., McCarter G., Levine J.D. Nitric oxide signaling in pain and nociceptor sensitization in the rat. J Neurosci 1998, 18(17):7008-7014.
2. Antonov I., Ha T., Antonova I., Moroz L.L., Hawkins R.D. Role of nitric oxide in classical conditioning of siphon withdrawal in Aplysia. J Neurosci 2007, 27(41):10993-101002.
3. Bach K.B., Mitchell G.S. Hypoxia-induced long-term facilitation of respiratory activity is serotonin dependent. Respir Physiol 1996, 104:251-260.
4. Baker-Herman T., Mitchell G.S. Phrenic long-term facilitation requires spinal serotonin receptor activation and protein synthesis. J Neurosci 2002, 22(14):6239-6246.
5. Baker-Herman T.L., Fuller D.D., Bavis R.W., Zabka A.G., Golder F.J., Doperalski N.J., Johnson R.A., Watters J.J., Mitchell G.S. BDNF is necessary and sufficient for spinal respiratory plasticity following intermittent hypoxia. Nat Neurosci 2004, 7(1):48-55.
6. Bliss T.V., Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 1993, 361:31-91.
7. Bryan-Lluka L.J., Papacostas M.H., Paczkowski F.A., Wanstall J.C. Nitric oxide donors inhibit 5-hydroxytrptamine (5-HT) uptake by the human 5-HT transporter (SERT). Brit J Pharmacol 2004, 143:63-70.
8. Chanrion B., Mannoury la Cour C., Bertaso F., Lerner-Natoli M., Freissmuth M., Millan M.J., Bockaert J., Marin P. Physical interaction between the serotonin transporter and neuronal nitric oxide synthase underlies reciprocal modulation of their activity. Proc Natl Acad Sci U S A 2007, 104(19):8119-8124.
9. Chiavegatto S., Nelson R.J. Interaction of nitric oxide and serotonin in aggressive behavior. Horm Behav 2003, 44(3):233-241.
10. Chugh D.K., Katayama M., Mokashi A., Bebout D.E., Ray D.K., Lahiri S. Nitric oxide-related inhibition of carotid chemosensory nerve activity in the cat. Respir Physiol 1994, 97(2):147-156.
11. Dale-Nagle E.A., Satriotomo I., Mitchell G.S. Multiple pathways to long-lasting phrenic motor facilitation. Adv Exp Med Biol 2010, 669:225-230.
12. Fuller D.D., Zabka A.G., Baker T.L., Mitchell G.S. Phrenic long-term facilitation requires 5-HT receptor activation during but not following episodic hypoxia. J Appl Physiol 2001, 90:2001-2006.
13. Fuller D.D., Johnson S.M., Olson E.B., Mitchell G.S. Synaptic pathways to phrenic motoneurons are enhanced by chronic intermittent hypoxia after cervical spinal cord injury. J Neurosci. 2003, 23(7):2993-3000.
14. Garthwaite J. Glutamate, nitric oxide and cell-cell signaling in the nervous system. Trends Neursci 1991, 14(2):60-67.
15. Garthwaite J. Concepts of neural nitric oxide-mediated transmission. Eur J Neurosci 2008, 27(11):2783-2802.
16. Gozal D., Gozal E. Episodic hypoxia enhances late hypoxic ventilation in developing rat: putative role of neuronal NO synthase. Am J Physiol Reg Int Comp Physiol 1999, 276:17-22.
17. Gozal D., Gozal E., Simakajornboon N. Signaling pathways of the acute hypoxic ventilatory response in the nucleus tractus solitarius. Respir Physiol 2000, 121(2-3):209-221.
18. Harkin A., Connor T.J., Walsh M., St John N., Kelly J.P. Serotonergic mediation of the antidepressant-like effects of nitric oxide synthase inhibitors. Neuropharmacology 2003, 44(5):616-623.
19. Hoffman M.S., Mitchell G.S. Spinal PKA inhibits phrenic long-term facilitation following acute intermittent hypoxia. Soc Neurosci 2008, Program No. 571.8.
20. Hoffman M.S., Nichols N.L., MacFarlane P.M., Mitchell G.S. Phrenic long-term facilitation after acute intermittent hypoxia requires spinal ERK activation, but not TrkB synthesis. J Appl Physiol 2012, 113(8):1184-1193.
21. Inan S.Y., Yalcin I., Aksu F. Dual effects of nitric oxide in the mouse forced swimming test: possible contribution of nitric oxide-mediated serotonin release and potassium modulation. Pharmacol Biochem Behav 2004, 77(3):457-464.
22. Kandel E.R. Cellular mechanisms of learning and the biological basis of individuality. Principles of neural science 2000, 1247-1279. McGraw-Hill, New York. E.R. Kandel, J.H. Schwartz, T.M. Jessell (Eds.).
23. Kim J.-S., Diebold B.A., Babior B.M., Knaus U.G., Bokoch G.M. Regulation of NOX1 activity via protein kinase A-mediated phosphorylation of NoxA1 and 14-3-3 binding. J Biol Chem 2007, 282(48):34787-34800.
24. Klann E., Thiels E. Modulation of protein kinases and protein phosphatases by reactive oxygen species: implications for hippocampal synaptic plasticity. Prog Neuropsychopharmacol Biol Psychiatry 1999, 23(3):359-376.
25. Klann E., Roberson E.D., Knapp L.T., Sweatt J.D. A role for superoxide in protein kinase C activation and induction of long-term potentiation. J Biol Chem 1998, 273(8):4516-4522.
26. Kline D.D., Overholt J.L., Prabhakar N.R. Mutant mice deficient in NOS-1 exhibit attenuated long-term facilitation and short term potentiation in breathing. J Physiol 2002, 539:309-315.
27. Knowles R.G. Nitric oxide biochemistry. Biochem Soc Trans 1997, 25(3):895-901.
28. Ling L. Serotonin and NMDA receptors in respiratory long-term facilitation. Respir Physiol Neurobiol 2008, 164(1-2):233-241.
29. Ling L., Fuller D.D., Bach K.B., Kinkead R., Olson E.B., Mitchell G.S. Chronic intermittent hypoxia elicits serotonin-dependent plasticity in the central neural control of breathing. J Neurosci 2001, 21(14):5381-5388.
30. MacFarlane P.M., Mitchell G.S. Respiratory long-term facilitation following intermittent hypoxia requires reactive oxygen species formation. Neurosci 2008, 152(1):189-197.
31. MacFarlane P.M., Mitchell G.S. Episodic spinal serotonin receptor activation elicits long-lasting phrenic motor facilitation by an NADPH oxidase-dependent mechanism. J Physiol 2009, 587(Pt 22):5469-5481.
32. MacFarlane P.M., Wilkerson J.E.R., Lovett-Barr M.R., Mitchell G.S. Reactive oxygen species and respiratory plasticity following intermittent hypoxia. Respir Physiol Neurobiol 2008, 164:263-271.
33. MacFarlane P.M., Satriotomo I., Windelborn J.A., Mitchell G.S. NADPH oxidase activity is necessary for acute intermittent hypoxia-induced phrenic long-term facilitation. J Physiol 2009, 587(9):1931-1942.
34. MacFarlane P.M., Vinit S., Mitchell G.S. Serotonin 2A and 2B receptor-induced phrenic motor facilitation: differential requirement for spinal NADPH oxidase activity. Neuroscience 2011, 178:45-55.
35. Maggi C.A., Meli A. Suitability of urethane anesthesia for physiopharmacological investigations. Part 3: Other systems. Experientia 1986, 42(5):531-537.
36. Mahamed S., Mitchell G.S. Is there a link between intermittent hypoxia-induced respiratory plasticity and obstructive sleep apnea?. Exp Physiol 2007, 92(1):27-37.
37. Mantilla C.B., Zhan W.Z., Sieck G.C. Retrograde labeling of phrenic motoneurons by intrapleural injection. J Neurosci Methods 2009, 182(2):244-249.
38. Marcus N.J., Li Y.L., Bird C.E., Schultz H.D., Morgan B.J. Chronic intermittent hypoxia augments chemoreflex control of sympathetic activity: role of the angiotensin II type 1 receptor. Resp Physiol Neurobiol 2010, 171(1):36-45.
39. McGuire M., Zhang Y., White D.P., Ling L. Serotonin receptor subtypes required for ventilatory long-term facilitation and its enhancement after chronic intermittent hypoxia in awake rats. Am J Physiol Integr Comp Physiol 2004, 286(2):R334-R341.
40. McGuire M., Zhang Y., White D.P., Ling L. Phrenic long-term facilitation requires NMDA receptors in the phrenic motonucleus in rats. J Physiol 2005, 567(Pt. 2):599-611.
41. Mitchell G.S., Baker T.L., Nanda S.A., Fuller D.D., Zabka A.G., Hodgeman B.A., Bavis R.W., Mack K.J., Olson E.B. Invited review: Intermittent hypoxia and respiratory plasticity. J Appl Physiol 2001, 90:2466-2475.
42. Nicoll R.A., Malenka R.C. Expression mechanisms underlying NMDA receptor-dependent long-term potentiation. Ann N Y Acad Sci 1999, 868:515-525.
43. Peng Y.J., Overholt J.L., Kline D., Kumar G.K., Prabhakar N.R. Induction of sensory long-term facilitation in the carotid body of intermittent hypoxia: implications for recurrent apneas. PNAS 2003, 100(17):10073-10078.
44. Peng Y.J., Yuan G., Jacono F.J., Kumar G.K., Prabhakar N.R. 5-HT evokes sensory long-term facilitation of rodent carotid body via activation of NADPH oxidase. J Physiol 2006, 576(1):289-295.
45. Pitsikas N., Tsitsirigou S., Zisopoulou S., Sakellaridis N. The 5-HT1A receptor and recognition memory. Possible modulation of its behavioural effects by the nitrergic system. Behav Brain Res 2005, 159(2):287-293.
46. Prabhakar N.R., Kumar G.K., Chang C.H., Agani F.H., Haxhiu M.A. Nitric oxide in the sensory function of the carotid body. Brain Res 1993, 625(1):16-22.
47. Shibuki K., Okada D. Endogenous nitric oxide release required for long-term synaptic depression in the cerebellum. Nature 1991, 349:326-328.
48. Son H., Hawkins R.D., Martin K., Kiebler M., Huang P.L., Fishman M.C. Long-term potentiation is reduced in mice that are doubly mutant in endothelial and neuronal nitric oxide synthase. Cell 1996, 87:1015-1023.
49. Straub V.A., Grant J., O'shea M., Benjamin P.R. Modulation of serotonergic neurotransmission by nitric oxide. J Neurophysiol 2007, 97:1088-1099.
50. Stuehr D.J. Mammalian nitric oxide synthases. Biochem Biophys Acta 1999, 1411(2-3):217-230.
51. Summers B.A., Overholt J.L., Prabhakar N.R. Nitric oxide inhibits L-type Ca2+ current in glomus cells of rabbit carotid body via a cGMP-independent mechanism. J Neurophysiol 1999, 81(4):1449-1457.
52. Torres J.E., Kreisman N.R., Gozal D. Nitric oxide modulates in vitro intrinsic optical signal and neural activity in the nucleus tractus solitaries of the rat. Neursci Lett 1997, 232(3):175-178.
53. Wilkerson J.E.R., Baker-Herman T.L., Mitchell G.S. Okadaic acid-sensitive protein phosphatases constrain phrenic long-term facilitation following sustained hypoxia. FASEB J 2008.