NADPH oxidase activity is necessary for acute intermittent hypoxia-induced phrenic long-term facilitation

Journal of Physiology

Volumn 587, Issue 9, 2009, Pages 1931-1942

  Macfarlane, P M ^a   Satriotomo, I ^a   Windelborn, J A ^a   Mitchell, G S ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOCYNIN; DIPHENYLIODONIUM SALT; MEMBRANE PROTEIN; PROTEIN P47PHOX; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; UNCLASSIFIED DRUG; PROTEIN P47; PROTEIN P47 PHOX; RAC1 PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CONTROLLED STUDY; CYTOSOL; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME LOCALIZATION; FACILITATION; HYPOGLOSSAL NERVE; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MALE; MICROGLIA; MOTONEURON; NERVE CELL MEMBRANE; NERVE CELL PLASTICITY; NONHUMAN; PHRENIC NERVE; PRIORITY JOURNAL; RAT; SPINAL CORD VENTRAL HORN; AMPLITUDE MODULATION; ANIMAL CELL; INTERMITTENT HYPOXIA; NEUROPHYSIOLOGY; PHRENIC LONG TERM FACILITATION; PROTEIN EXPRESSION;

ANIMALS; ENZYME ACTIVATION; LONG-TERM POTENTIATION; MALE; MOTOR NEURONS; NADPH OXIDASE; NEURONAL PLASTICITY; OXYGEN; PHRENIC NERVE; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES;

EID: 65449179933     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2008.165597     Document Type: Article

References (43)

1. Abramov AY, Scorziello A & Duchen MR (2007). Three distinct mechanisms generate oxygen free radicals in neurons and contribute to cell death during anoxia and reoxygenation. J Neurosci 27, 1129-1138.
2. Baker TL & Mitchell GS (2000). Episodic but not continuous hypoxia elicits long-term facilitation of phrenic motor output in rats. J Physiol 15, 215-219.
3. Baker-Herman T & Mitchell GS (2002). Phrenic long-term facilitation requires spinal serotonin receptor activation and protein synthesis. J Neurosci 22, 6239-6246.
4. Baker-Herman TL, Fuller DD, Bavis RW, Zabka AG, Golder FJ, Doperalski NJ, Johnson RA, Watters JJ & Mitchell GS (2004). BDNF is necessary and sufficient for spinal respiratory plasticity following intermittent hypoxia. Nat Neurosci 7, 48-55.
5. Dinger B, He L, Chen J, Liu X, Gonzalez C, Obeso A, Sanders K, Hoidal J, Stensaas L & Fidone S (2007). The role of NADPH oxidase in carotid body arterial chemoreceptors. Respir Physiol Neurobiol 157, 45-54.
6. Erickson JT & Millhorn DE (1994). Hypoxia and electrical stimulation of the carotid sinus nerve induce Fos-like immunoreactivity within catecholaminergic and serotoninergic neurons of the rat brainstem. J Comp Neurol 348, 161-182.
7. Feldman JL, Mitchell GS & Nattie EE (2003). Breathing: Rhythmicity, plasticity, chemosensitivity. Annu Rev Neurosci 26, 239-266.
8. Fuller DD, Bach KB, Baker TL, Kinkead R & Mitchell GS (2000). Long term facilitation of phrenic nerve output. Respir Physiol 121, 135-146.
9. Fuller DD, Baker TL, Behan M & Mitchell GS (2001a). Expression of hypoglossal long-term facilitation differs between substrains of Sprague-Dawley rat. Physiol Genomics 4, 175-181.
10. Fuller DD, Zabka AG, Baker TL & Mitchell GS (2001b). Selected contribution: Phrenic long-term facilitation requires 5-HT receptor activation during but not following episodic hypoxia. J Appl Physiol 90, 2001-2006.
11. Glass MJ, Huang J, Oselkin M, Tarsitano MJ, Wang G, Iadecola C & Pickel VM (2006). Subcellular localization of nicotinamide adenine dinucleotide phosphate oxidase subunits in neurons and astroglia of the rat medial nucleus tractus solitarius: Relationship with tyrosine hydroxylase immunoreactive neurons. Neurosci 143, 547-564.
12. Green PS, Mendez AJ, Jacob JS, Crowley JR, Growdon W, Hyman BT & Heinecke JW (2004). Neuronal expression of myeloperoxidase is increased in Alzheimers disease. J Neurochem 90, 724-733.
13. Grewal JS, Mukhin YV, Gamovskaya MN, Raymond JR & Greene EL (1999). Serotonin 5-HT2A receptor induces TGF-β1 expression in mesangial cells via ERK: Proliferative and fibrotic signals. Am J Physiol Renal Physiol 276, F922-F930.
14. Heumüller S, Wind S, Barbosa-Sicard E, Schmidt HH, Busse R, Schröder K & Brandes RP (2008). Apocynin is not an inhibitor of vascular NADPH oxidases but an antioxidant. Hypertension 51, 211-217.
15. Kinkead R & Mitchell GS (1999). Time-dependent hypoxic ventilatory responses in rats: Effects of ketanserin and 5-carboxyamidotryptamine. Am J Physiol Regul Integr Comp Physiol 277, R658-R666.
16. Kinkead R, Bach KB, Johnson SM, Hodgeman BA & Mitchell GS (2001). Plasticity in respiratory motor control: Intermittent hypoxia and hypercapnia activate opposing serotonergic and noradrenergic modulatory systems. Comp Biochem Physiol A Mol Integr Physiol 130, 207-218.
17. Kishida KT, Hoeffer CA, Hu D, Pao M, Holland SM & Klann E (2006). Synaptic plasticity deficits and mild memory impairments in mouse models of chronic granulomatous disease. Mol Cell Biol 26, 5908-5920.
18. Kishida KT & Klann E (2007). Sources and targets of reactive oxygen species in synaptic plasticity and memory. Antiox Redox Signal 9, 233-244.
19. Klann E, Roberson ED, Knapp LT & Sweatt JD (1998). A role for superoxide in protein kinase C activation and induction of long-term potentiation. J Biol Chem 273, 4516-4522.
20. Klann E & Thiels E (1999). Modulation of protein kinases and protein phosphatases by reactive oxygen species: Implications for hippocampal synaptic plasticity. Prog Neuropsychopharmacol Biol Psychiatry 23, 359-376.
21. MacFarlane PM & Mitchell GS (2007). Serotonin-induced phrenic long-term facilitation requires reactive oxygen species signalling via the NADPH oxidase complex. Abstract SFN.
22. MacFarlane PM, Satriotomo I & Mitchell GS (2007). Reactive oxygen species generated by NADPH oxidase are necessary for phrenic long-term facilitation following acute intermittent hypoxia. FASEB J.
23. MacFarlane PM & Mitchell GS (2008). Respiratory long-term facilitation following intermittent hypoxia requires reactive oxygen species formation. Neurosci 152, 189-197.
24. MacFarlane PM, Wilkerson JE, Lovett-Barr MR & Mitchell GS (2008). Reactive oxygen species and respiratory plasticity following intermittent hypoxia. Respir Physiol Neurobiol 164, 263-271.
25. Maggi CA & Meli A (1986). Suitability of urethane anesthesia for physiopharmacological investigations in various systems. Part 1: General considerations. Experientia 42, 109-114.
26. Mahamed S & Mitchell GS (2007). Is there a link between intermittent hypoxia-induced respiratory plasticity and obstructive sleep apnoea? Exp Physiol 92, 27-37.
27. McGuire M & Ling L (2004). Activation of protein kinase C near/in phrenic motoneurons is required for phrenic long-term facilitation in rats. Am J Respir Crit Care Med 169, A433.
28. Mitchell GS, Baker TL, Nanda SA, Fuller DD, Zabka AG, Hodgeman BA, Bavis RW, Mack KJ & Olson EB Jr (2001). Intermittent hypoxia and respiratory plasticity. J Appl Physiol 90, 2466-2475.
29. Mitchell GS & Johnson SM (2003). Neuroplasticity in respiratory motor control. J Appl Physiol 94, 358-374.
30. Mitchell GS (2007). Respiratory plasticity following intermittent hypoxia: A guide for novel therapeutic approaches to ventilatory control disorders. In Genetic Basis for Respiratory Control Disorders, ed. Gaultier C, pp. 291-311. Springer, New York.
31. Morris KF, Arata A, Shannon R & Lindsey BG (1996). Long-term facilitation of phrenic nerve activity in cats: Responses and short time scale correlations of medullary neurons. J Physiol 490, 463-480.
32. Nakayama T, Harada N, Asano M, Nomura N, Saito T, Mishima A & Okajima K (2007). Atrial natriuretic peptide reduces ischemia/ reperfusion-induced spinal cord injury in rats by enhancing sensory neuron activation. J Pharmacol Exp Ther 322, 582-590.
33. Neverova NV, Saywell SA, Nashold LJ, Mitchell GS & Feldman JL (2007). Episodic stimulation of α1-adrenoreceptors induces protein kinase C-dependent persistent changes in motoneuronal excitability. J Neurosci 27, 4435-4442
34. O'Donnell BV, Tew DG, Jones OT & England PJ (1993). Studies on the inhibitory mechanism of iodonium compounds with special reference to neutrophil NADPH oxidase. Biochem J 290, 41-49.
35. Peng YJ, Overholt JL, Kline D, Kumar GK & Prabhakar NR (2003). Induction of sensory long-term facilitation in the carotid body of intermittent hypoxia: Implications for recurrent apneas. Proc Natl Acad Sci U S A 100, 10073-10078.
36. Peng YJ, Yuan G, Jacono FJ, Kumar GK & Prabhakar NR (2006). 5-HT evokes sensory long-term facilitation of rodent carotid body via activation of NADPH oxidase. J Physiol 576, 289-295.
37. Sanders KA, Sundar KM, He L, Dinger B, Fidone S & Hoidal JR (2002). Role of components of the phagocytic NADPH oxidase in oxygen sensing. J Appl Physiol 93, 357-364.
38. + -ATPase. J Biol Chem 283, 27982-27990.
39. Tejada-Simon MV, Serrano F, Villasana LE, Kanterewicz BI, Wu GY, Quinn MT & Klann E (2005). Synaptic localization of a functional NADPH oxidase in the mouse hippocampus. Mol Cell Neurosci 29, 97-106.
40. Teppema LJ, Veening JG, Kranenburg A, Dahan A, Berkenbosch A & Olievier C (1997). Expression of c-fos in the rat brainstem after exposure to hypoxia and to normoxic and hyperoxic hypercapnia. J Comp Neurol 388, 169-190.
41. Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M & Telser J (2007). Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39, 44-84.
42. Wilkerson JER, MacFarlane PM, Hoffman MS & Mitchell GS (2007). Respiratory plasticity following intermittent hypoxia: Roles of protein phosphatases and reactive oxygen species. Biochem Soc Trans 35, 1269-1272.
43. Wilkerson JER, Satriotomo I, Baker-Herman TL, Watters TL & Mitchell GS (2008). Okadaic acid-sensitive protein phosphatases constrain phrenic long-term facilitation after sustained hypoxia. J Neurosci 28, 2949-2958.