Adenosine 2A receptor inhibition enhances intermittent hypoxia-induced diaphragm but not intercostal long-term facilitation

Journal of Neurotrauma

Volumn 31, Issue 24, 2014, Pages 1975-1984

  Navarrete Opazo, Angela A ^a   Vinit, Stéphane ^b   Mitchell, Gordon S ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE RECEPTOR;

ANIMAL; ANOXIA; DIAPHRAGM; INNERVATION; INTERCOSTAL MUSCLE; LONG TERM POTENTIATION; MALE; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; RAT; RESPIRATORY FUNCTION; SPINAL CORD INJURY; SPRAGUE DAWLEY RAT;

ANIMALS; ANOXIA; DIAPHRAGM; INTERCOSTAL MUSCLES; LONG-TERM POTENTIATION; MALE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, PURINERGIC P1; RESPIRATORY PHYSIOLOGICAL PHENOMENA; SPINAL CORD INJURIES;

EID: 84914155822     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2014.3393     Document Type: Article

References (39)

1. Mitchell, G.S., and Johnson, S.M. (2003). Neuroplasticity in respiratory motor control. J. Appl. Physiol. 94, 358-374.
2. Mahamed, S., and Mitchell, G.S. (2007). Is there a link between intermittent hypoxia-induced respiratory plasticity and obstructive sleep apnoea? Exp. Physiol. 92, 27-37.
3. Terada, J., and Mitchell, G.S. (2011). Diaphragm long-Term facilitation following acute intermittent hypoxia during wakefulness and sleep. J. Appl. Physiol. 110, 1299-1310.
4. Devinney, M.J., Huxtable, A.G., Nichols, N.L., and Mitchell, G.S. (2013). Hypoxia-induced phrenic long-Term facilitation: Emergent properties. Ann. N.Y. Acad. Sci. 1279, 143-153.
5. Navarrete-Opazo, A., and Mitchell, G. (2013). Inspiratory intercostal long term facilitation in unanesthetized rats. In: Experimental Biology. FASEB J: Boston.
6. Dale-Nagle, E.A., Hoffman, M.S., MacFarlane, P.M. and Mitchell, G.S. (2010). Multiple pathways to long-lasting phrenic motor facilitation. Exp. Med. Biol. 669, 225-230.
7. Nichols, N.L., Dale, E.A., and Mitchell, G.S. (2012). Severe acute intermittent hypoxia elicits phrenic long-Term facilitation by a novel adenosine-dependent mechanism. J. Appl. Physiol. 112, 1678-1688.
8. Baker-Herman, T.L., and Mitchell, G.S. (2002). Phrenic long-Term facilitation requires spinal serotonin receptor activation and protein synthesis. J. Neurosci. 22, 6239-6246.
9. Feldman, J.L., Mitchell, G.S., and Nattie, E.E. (2003). Breathing: Rhythmicity, plasticity, chemosensitivity. Ann. Rev. Neurosci. 26, 239-266.
10. 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., and Mitchell, G.S. (2004). BDNF is necessary and sufficient for spinal respiratory plasticity following intermittent hypoxia. Nat. Neurosci. 7, 48-55.
11. Feldman, J.L., Neverova, N.V., and Saywell, S.A. (2005). Modulation of hypoglossal motoneuron excitability by intracellular signal transduction cascades. Respir. Physiol Neurobiol 147, 131-143.
12. Hoffman, M.S., Golder, F.J., Mahamed, S., and Mitchell, G.S. (2010). Spinal adenosine A2(A) receptor inhibition enhances phrenic long term facilitation following acute intermittent hypoxia. J. Physiol. 588, 255-266.
13. Golder, F.J., and Mitchell, G.S. (2005). Spinal synaptic enhancement with acute intermittent hypoxia improves respiratory function after chronic cervical spinal cord injury. J. Neurosci. 25, 2925-2932.
14. Lovett-Barr, M.R., Satriotomo, I., Muir, G.D., Wilkerson, J.E., Hoffman, M.S., Vinit, S., and Mitchell, G.S. (2012). Repetitive intermittent hypoxia induces respiratory and somatic motor recovery after chronic cervical spinal injury. J. Neurosci. 32, 3591-3600.
15. Mitchell, G.S., Baker, T.L., Nanda, S.A., Fuller, D.D., Zabka, A.G., Hodgeman, B.A., Bavis, R.W., Mack, K.J., and Olson, E.B., Jr. (2001). Invited review: Intermittent hypoxia and respiratory plasticity. J. Appl. Physiol. 90, 2466-2475.
16. Food and Drug Administration. (2001). Guidance for Industry. S7A Safety Pharmacology Studies for Human Pharmaceuticals. U.S. Department of Health and Human Services. Rockville, Md.
17. Vinit, S., Lovett-Barr, M.R., and Mitchell, G.S. (2009). Intermittent hypoxia induces functional recovery following cervical spinal injury. Respir. Physiol. Neurobiol. 169, 210-217.
18. Fuller, D.D., Sandhu, M.S., Doperalski, N.J., Lane, M.A., White, T.E., Bishop, M.D., and Reier, P.J. (2009). Graded unilateral cervical spinal cord injury and respiratory motor recovery. Respir. Physiol. Neurobiol. 165, 245-253.
19. Yang, M., Soohoo, D., Soelaiman, S., Kalla, R., Zablocki, J., Chu, N., Leung, K., Yao, L., Diamond, I., Belardinelli, L., and Shryock, J.C. (2007). Characterization of the potency, selectivity, and pharmacokinetic profile for six adenosine A2A receptor antagonists. Naunyn Schmiedebergs Arch. Pharmacol. 375, 133-144.
20. Paxinos, G., and Watson, C. (1998 ). The Rat Brain in Stereotaxic Coordinates. 4th ed. Academic Press: Waltham, MA.
21. Vinit, S., Gauthier, P., Stamegna, J.C., and Kastner, A. (2006). High cervical lateral spinal cord injury results in long-Term ipsilateral hemidiaphragm paralysis. J. Neurotrauma 23, 1137-1146.
22. Legrand, A., and De Troyer, A. (1999). Spatial distribution of external and internal intercostal activity in dogs. J. Physiol. 518, 291-300.
23. Dougherty, B.J., Lee, K.Z., Gonzalez-Rothi, E.J., Lane, M.A., Reier, P.J., and Fuller, D.D. (2012). Recovery of inspiratory intercostal muscle activity following high cervical hemisection. Respir. Physiol. Neurobiol. 183, 186-192.
24. Baker-Herman, T.L., and Strey, K.A. (2011). Similarities and differences in mechanisms of phrenic and hypoglossal motor facilitation. Respir. Physiol. Neurobiol. 179, 48-56.
25. Golder, F.J., Ranganathan, L., Satriotomo, I., Hoffman, M., Lovett-Barr, M.R., Watters, J.J., Baker-Herman, T.L., and Mitchell, G.S. (2008). Spinal adenosine A2a receptor activation elicits long-lasting phrenic motor facilitation. J. Neurosci. 28, 2033-2042.
26. Hoffman, M.S., and Mitchell, G.S. (2013). Spinal 5-HT7 receptors and protein kinase A constrain intermittent hypoxia-induced phrenic longterm facilitation. Neuroscience 250, 632-643.
27. Kirkwood, P.A., Munson, J.B., Sears, T.A., and Westgaard, R.H. (1988). Respiratory interneurones in the thoracic spinal cord of the cat. J. Physiol. 395, 161-192.
28. Kirkwood, P.A., Schmid,K., and Sears, T.A. (1993). Functional identities of thoracic respiratory interneurones in the cat. J. Physiol. 461, 667-687.
29. Nantwi, K.D., El-Bohy, A.A., Schrimsher, G.W., Reier, P.J., and Goshgarian, H.G. (1999). Spontaneous functional recovery in a paralyzed hemidiaphragm following upper cervical spinal cord injury in adult rats. Neurorehab. Neural Repair 13, 225-234.
30. Fuller, D.D., Golder, F.J., Olson, E.B., Jr., and Mitchell, G.S. (2006). Recovery of phrenic activity and ventilation after cervical spinal hemisection in rats. J. Appl. Physiol. 100, 800-806.
31. Dougherty, B.J., Lee, K.Z., Lane, M.A., Reier, P.J., and Fuller, D.D. (2012). Contribution of the spontaneous crossed-phrenic phenomenon to inspiratory tidal volume in spontaneously breathing rats. J. Appl. Physiol. 112, 96-105.
32. Goshgarian, H.G. (2003). The crossed phrenic phenomenon: A model for plasticity in the respiratory pathways following spinal cord injury. J. Appl. Physiol. 94, 795-810.
33. Ling, L., Bach, K.B., and Mitchell, G.S. (1994). Serotonin reveals ineffective spinal pathways to contralateral phrenic motoneurons in spinally hemisected rats. Exp. Brain Res. 101, 35-43.
34. Saywell, S.A., Ford, T.W., Meehan, C.F., Todd, A.J., and Kirkwood, P.A. (2011). Electrophysiological and morphological characterization of propriospinal interneurons in the thoracic spinal cord. J. Neurophysiol. 105, 806-826.
35. Teitelbaum, J., Borel, C.O., Magder, S., Traystman, R.J., and Hussain, S.N. (1993). Effect of selective diaphragmatic paralysis on the inspiratory motor drive. J. Appl. Physiol. 74, 2261-2268.
36. Katagiri, M., Young, R.N., Platt, R.S., Kieser, T.M., and Easton, P.A. (1994). Respiratory muscle compensation for unilateral or bilateral hemidiaphragm paralysis in awake canines. J. Appl. Physiol. 77, 1972-1982.
37. Brichant, J.F., and De Troyer, A. (1997). On the intercostal muscle compensation for diaphragmatic paralysis in the dog. J. Physiol. 500, 245-253.
38. Golder, F.J., Fuller, D.D., Davenport, P.W., Johnson, R.D., Reier, P.J., and Bolser, D.C. (2003). Respiratory motor recovery after unilateral spinal cord injury: Eliminating crossed phrenic activity decreases tidal volume and increases contralateral respiratory motor output. J. Neurosci. 23, 2494-2501.
39. Mitchell, G. (2007). Respiratory plasticity following intermittent hypoxia: A guide for novel therapeutic approaches to ventilatory control disorders. In: Genetic Basis for Respiratory Control Disorders. Gaultier, C. (ed). Springer Publishing Company: New York, pps. 291-311.