Inhibition of protein kinase G activity protects neonatal mouse respiratory network from hyperthermic and hypoxic stress

Brain Research

Volumn 1311, Issue , 2010, Pages 64-72

  Armstrong, Gary A B ^a   López Guerrero, Juan J ^b   Dawson Scully, Ken ^c   Peña, Fernando ^b   Robertson, R Meldrum ^a  

^a QUEEN S UNIVERSITY   (Canada)

^b DEPARTAMENTO DE FÍSICA   (Mexico)

^c FLORIDA ATLANTIC UNIVERSITY   (United States)

Author keywords

Hyperthermia; Hypoxia; Neonate; Neuronal circuit; PKG; Respiration

Indexed keywords

8 BROMO CYCLIC GMP; CYCLIC GMP DEPENDENT PROTEIN KINASE; KT 5823;

ANIMAL TISSUE; ARTICLE; BRAIN STEM; BREATHING PATTERN; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; HEAT SENSITIVITY; HYPERTHERMIA; HYPOXIA; MOUSE; NERVE CELL NETWORK; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY ARREST; RESPIRATORY NERVE CELL; STRESS; TEMPERATURE;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; BRAIN STEM; CARBAZOLES; CELL HYPOXIA; CYCLIC GMP; CYCLIC GMP-DEPENDENT PROTEIN KINASES; FEVER; MICE; MICE, INBRED STRAINS; MICROELECTRODES; NEURONS; PERIODICITY; PROTEIN KINASE INHIBITORS; RESPIRATION; TEMPERATURE;

INVERTEBRATA; MAMMALIA;

EID: 72649102342     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2009.11.038     Document Type: Article

References (60)

1. Armstrong G.A.B., and Robertson R.M. A role for octopamine in coordinating thermoprotection of an insect nervous system. J. Therm. Biol. 31 (2006) 149-158
2. Armstrong G.A.B., Shoemaker K.L., Money T.G.A., and Robertson R.M. Octopamine mediates thermal preconditioning of the locust ventilatory central pattern generator via a cAMP/protein kinase A signaling pathwa. J. Neurosci. 22 (2006) 12118-12126
3. Armstrong G.A.B., Rodgers C.I., Money T.G.A., and Robertson R.M. Suppression of spreading depression-like events in locusts by inhibition of the NO/cGMP/PKG pathway. J. Neurosci. 29 (2009) 8225-8235
4. + channels in rat hearts. Am. J. Physiol. Heart Circ. Physiol. 29 (2006) H1808-H1817
5. Czéh G., and Somjen G.G. Hypoxic failure of synaptic transmission in the isolated spinal cord, and the effects of divalent cations. Brain Res. 527 (1990) 224-233
6. Dawson-Scully K., Armstrong G.A., Kent C., Robertson R.M., and Sokolowski M.B. Natural variation in the thermotolerance of neural function and behavior due to a cGMP-dependent protein kinase. PloS ONE 2 (2007) e773
7. De Paula P.M., and Bronco L.G. Nitric oxide in the rostral ventrolateral medulla modulates hyperpnea but not anapyrexia induced by hypoxia. Brain Res. 977 (2003) 231-238
8. Doi A., and Ramirez J.M. Neuromodulation and the orchestration of the respiratory rhythm. Respir. Physiol. Neurobiol. 164 (2008) 96-104
9. Garthwaite J. Concepts of neural nitric oxide-mediated transmission. Eur. J. Neurosci. 27 (2008) 2783-2802
10. Guix F.X., Uribesalgo I., Coma M., and Muñoz F.J. The physiology and pathophysiology of nitric oxide in the brain. Prog. Neurobiol. 76 (2005) 126-152
11. El-Husseini A.E., Bladen C., and Vincent S.R. Molecular characterization of a type II cyclic GMP-dependent protein kinase expressed in the rat brain. J. Neurochem. 64 (1995) 2814-2817
12. El-Husseini A.E., Williams J., Reiner P.B., Pelech S., and Vincent S.R. Localization of the cGMP-dependent protein kinase in relation to nitric oxide synthase in the brain. J. Chem. Neuroanat. 16 (1999) 45-55
13. Fabris G., Steiner A.A., nselmo-Franci J.A., and Branco L.G. Role of nitric oxide in rat locus coeruleus in hypoxia-induced hyperventilation and hypothermia. Neuroreport 11 (2000) 2991-2995
14. Feldman J.L., and Del Negro C.A. Looking for inspiration: new perspectives on respiratory rhythm. Nat. Rev. Neurosci. 7 (2006) 232-242
15. Feldman J.L., Mitchell G.S., and Nattie E.E. Breathing: rhythmicity, plasticity, chemosensitivity. Annu. Rev. Neurosci. 26 (2003) 239-266
16. Feweel J.E. Protective responses of the newborn to hypoxia. Respir. Physiol. Neurobiol. 149 (2005) 243-255
17. Funke F., Kron M., Dutschmann M., and Müller M. Infant brainstem is prone to the generation of spreading depression during severe hypoxia. J. Neurophysiol. 101 (2009) 2395-2410
18. Gaston B., Singel D., Doctor A., and Stamler J.S. S-nitrosothiol signaling in respiratory biology. Am. J. Respir. Crit. Care Med. 173 (2006) 1186-1193
19. Gozal D., and Torres J.E. Brainstem nitric oxide tissue levels correlate with anoxia-induced gasping activity in the developing rat. Biol. Neonate 79 (2001) 122-130
20. Haxhiu M.A., Chang C.H., Dreshaj I.A., Erokwu B., Prabhakar N.R., and Cherniack N.S. Nitric oxide and ventilatory response to hypoxi. Respir. Physiol. 81 (1995) 257-266
21. Hedrick M.S., Morales R.D., Parker J.M., and Pacheco J.L.H. Nitric oxide modulates respiratory-related neural activity in the isolated brainstem of the bullfrog. Neurosci. Lett. 251 (1998) 81-84
22. Jia L., Bonaventura C., Bonaventura J., and Stamler J.S. S-nitrosohaemoglobin: a dynamic activity of blood involved in vascular control. Nature 380 (1996) 221-226
23. + currents in the presumed cholinergic neuron of basal forebrain. J. Neurophysiol. 98 (2007) 3397-3410
24. + channel in OK proximal tubule cells involves cGMP-dependent phosphorylation process. Jpn. J. Physiol. 48 (1998) 467-476
25. Lieske S.P., Thoby-Brisson M., Telgkamp P., and Ramirez J.M. Reconfiguration of the neural network controlling multiple breathing patterns: eupnea, sighs and gasps. Nat. Neurosci. 3 (2000) 600-607
26. Ling L., Karius D.R., Fiscus R.R., and Speck D.F. Endogenous nitric oxide required for an integrative respiratory function in the cat brain. J. Neurophysiol. 68 (1992) 1910-1912
27. Lipton A.J., Johnson M.A., Macdonald T., Lieberman M.W., Gozal D., and Gaston B. S-nitrosothiols signal the ventilatory response to hypoxi. Nature 413 (2001) 171-174
28. Moncada S., Palmer R.M., and Higgs E.A. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol. Rev. 43 (1991) 109-142
29. + concentrations, extra- and intracellular voltages, and the effect of TTX in hypoxic rat hippocampal slices. J. Neurophysiol. 83 (2000) 735-745
30. Newman A.E.M., Foerster M., Shoemaker K.L., and Robertson R.M. Stress-induced thermotolerance of ventilatory motor pattern generation in the locust, Locusta migratoria. J. Insect. Physiol. 49 (2003) 1039-1047
31. Osborne K.A., Robichon A., Burgess E., Butland S., Shaw R.A., Coulthard A., Pereira H.S., Greenspan R.J., and Sokolowski M.B. Natural behavior polymorphism due to a cGMP-dependent protein kinase of Drosophila. Science 277 (1997) 834-836
32. Peever J.H., Tian G.-F., and Duffin J. Temperature and pH affect respiratory rhythm of in-vitro preparations from neonatal rats. Resp. Physiol. 117 (1999) 97-107
33. Peña F., and Ramirez J.M. Endogenous activation of serotonin-2A receptors is required for respiratory rhythm generation in vitro. J. Neurosci. 22 (2002) 11055-11064
34. Peña F., Parkis M., Tryba A., and Ramirez J.M. Differential contribution of pacemaker properties to the generation of respiratory rhythms during normoxia and hypoxia. Neuron 84 (2004) 105-117
35. Peña F., Meza-Andrade R., Páez-Zayas V., and González-Marín M.C. Gasping generation in developing Swiss-Webster mice and in vitro and in vivo. Neurochem. Res. 33 (2008) 1492-1500
36. Pierrefiche O., Abdala A.P.L., and Paton J.F.R. Nitric oxide and respiratory rhythm in mammals: a new modulator of phase transition?. Biochem. Soc. Trans. 35 (2007) 1258-1263
37. Reeves S.R., Simakajornboon N., and Gozal D. The role of nitric oxide in the neuronal control of breathing. Resp. Physiol. Neurobiol. 164 (2008) 143-150
38. Rekling J.C., and Feldman J.L. PreBotzinger complex and pacemaker neurons: hypothesized site and kernel for respiratory rhythm generation. Annu. Rev. Physiol. 60 (1998) 385-405
39. Renger J.J., Yoa W.D., Sokolowski M.B., and Wu C.F. Neuronal polymorphism among natural alleles of a cGMP-dependent kinase gene, Foraging, in Drosophila. J. Neurosci. 19 (1999) RC28 (1999)
40. Ramirez J.M., Elsen F.P., and Robertson R.M. Long-term effects of prior heat shock on neuronal potassium currents recorded in a novel insect ganglion slice preparation. J. Neurophysiol. 81 (1999) 795-802
41. Richter F., Rupprecht S., Lemenkühler A., and Schaible H.G. Spreading depression can be elicited in brain stem of immature but not adult rats. J. Neurophysiol. 90 (2003) 2163-2170
42. Robertson R.M. Thermal stress and neural function: adaptive mechanisms in insect model systems. J. Therm. Biol. 29 (2004) 351-358
43. Rodgers C.I., Armstrong G.A.B., Shoemaker K.L., LaBrie J.D., Moyes C.D., and Robertson R.M. Stress preconditioning of spreading depression in the locust CNS. PloS ONE 2 (2007) e1366
44. Smith J.C., Ellenberger H.H., Ballanyi K., Ritcher D.W., and Feldman J.L. Pre-Bötzinger complex: a brainstem region that may generate respiratory rhythm in mammals. Science 254 (1991) 726-729
45. Somjen G.G. Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. Physiol. Rev. 81 (2001) 1065-1096
46. Sridhar R., Thach B.T., Kelly D.H., and Henslee J.A. Characterization of successful and failed autoresuscitation in human infants, including those dying of SIDS. Pediatr. Pulmonol. 36 (2003) 113-122
47. Streit D.S., Ferreira F., and Martins-Ferreira H. Spreading depression in isolated spinal cord. J. Neurophysiol. 74 (1995) 888-890
48. Tagawa T., Imaizumi T., Harada S., Endo T., Shiramoto M., Hirooka Y., and Takeshita A. Nitric oxide influences neuronal activity in the nucleus tractus solitarius of rat brainstem slice. Circ. Res. 75 (1994) 70-76
49. Takahashi H., Manaka S., and Sano K. Changes in extracellular potassium concentration in cortex and brain stem during the acute phase of experimental closed head injury. J. Neurosurg. 55 (1981) 708-717
50. Travagli R.A., and Gillis R.A. Nitric oxide-mediated excitatory effect on neurons of dorsal motor nucleus of vagus. Am. J. Physiol. 266 (1994) G154-G160
51. Tryba A.K., and Ramirez J.-M. Response of the respiratory network of mice to hyperthermia. J. Neurophysiol. 89 (2003) 2975-2983
52. Tryba A.K., and Ramirez J.-M. Hyperthermia modulates respiratory pacemaker bursting properties. J. Neurophysiol. 92 (2004) 2844-2852
53. 2A receptors. J. Neurosci. 26 (2006) 2623-2634
54. Vyskočil F., Kříž N., and Bureš J. Potassium-selective microelectrodes used for measuring the extracellular brain potassium during spreading and anoxic depolarization in rats. Brain Res. 39 (1972) 255-259
55. Wingrove J.A., and O'Farrell P.H. Nitric oxide contributes to behavioral, cellular, and developmental responses to low oxygen in Drosophila. Cell 98 (1999) 105-114
56. Wu J., and Fisher R.S. Hyperthermic spreading depression in the immature rat hippocampal slice. J. Neurophysiol. 84 (2000) 1355-1360
57. Wu B.S., Walker V.K., and Robertson R.M. Heat shock-induced thermoprotection of action potentials in the locust flight system. J. Neurobiol. 49 (2001) 188-199
58. Wu B.S., Lee J.K., Thompson K.M., Walker V.K., Moyes C.D., and Robertson R.M. Anoxia induces thermotolerance in the locust flight system. J. Exp. Biol. 205 (2002) 815-827
59. Xu Z.Q., de Vente J., Steinbusch H., Grillner S., and Hokfelt T. The NO-cGMP pathway in the rat locus coeruleus: electrophysiological, immunohistochemical and in situ hybridization studies. Eur. J. Neurosci. 10 (1998) 3508-3516
60. Yetik-Anacak G., and Catravas J.D. Nitric oxide and the endothelium: history and impact on cardiovascular disease. Vascul. Pharmacol. 45 (2006) 268-276