Glial-derived adenosine modulates spinal motor networks in mice

Journal of Neurophysiology

Volumn 107, Issue 7, 2012, Pages 1925-1934

  Witts, Emily C ^a   Panetta, Kara M ^a   Miles, Gareth B ^a  

^a UNIVERSITY OF ST ANDREWS   (United Kingdom)

Author keywords

Motor control; Neuromodulation; Spinal cord

Indexed keywords

ADENOSINE; ADENOSINE RECEPTOR BLOCKING AGENT; BETA,GAMMA DIBROMOMETHYLENE 6 N,N DIETHYLADENOSINE TRIPHOSPHATE; PROTEIN KINASE; THEOPHYLLINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; LOCOMOTION; MOTOR CONTROL; MOUSE; NERVE CELL NETWORK; NEUROMODULATION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; SPINAL CORD; SPINAL MOTOR NETWORK; VENTRAL ROOT;

ADENOSINE; ADENOSINE TRIPHOSPHATE; ANALGESICS; ANIMALS; ANIMALS, NEWBORN; ENZYME INHIBITORS; MICE; MICE, INBRED C57BL; MOTOR NEURONS; NERVE NET; PERIODICITY; PURINERGIC ANTAGONISTS; SPINAL CORD;

EID: 84859538274     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00513.2011     Document Type: Article

References (58)

1. Alvarez FJ, Jonas PC, Sapir T, Hartley R, Berrocal MC, Geiman EJ, Todd AJ, Goulding M. Postnatal phenotype and localization of spinal cord V1 derived interneurons. J Comp Neurol 493: 177-192, 2005.
2. Banner KH, Page CP. Theophylline and selective phosphodiesterase inhibitors as anti-inflammatory drugs in the treatment of bronchial asthma. Eur Respir J 8: 996-1000, 1995.
3. Bracci E, Ballerini L, Nistri A. Spontaneous rhythmic bursts induced by pharmacological block of inhibition in lumbar motoneurons of the neonatal rat spinal cord. J Neurophysiol 75: 640-647, 1996.
4. 2+ currents and motor pattern generation in the xenopus embryo. J Physiol 525: 655-667, 2000.
5. Brown P, Dale N. Modulation of K(+) currents in Xenopus spinal neurons by p2y receptors: a role for ATP and ADP in motor pattern generation. J Physiol 540: 843-850, 2002.
6. Burnstock G. Noradrenaline and ATP: cotransmitters and neuromodulators. J Physiol Pharmacol 46: 365-384, 1995.
7. Burnstock G. Physiology and pathophysiology of purinergic neurotransmission. Physiol Rev 87: 659-797, 2007.
8. Clarke DD. Fluoroacetate and fluorocitrate: mechanism of action. Neurochem Res 16: 1055-1058, 1991.
9. Cunha RA. Adenosine as a neuromodulator and as a homeostatic regulator in the nervous system: different roles, different sources and different receptors. Neurochem Int 38: 107-125, 2001.
10. Dale N. Delayed production of adenosine underlies temporal modulation of swimming in frog embryo. J Physiol 511: 265-272, 1998.
11. Dale N, Gilday D. Regulation of rhythmic movements by purinergic neurotransmitters in frog embryos. Nature 383: 259-263, 1996.
12. Deuchars SA, Brooke RE, Deuchars J. Adenosine A1 receptors reduce release from excitatory but not inhibitory synaptic inputs onto lateral horn neurons. J Neurosci 21: 6308-6320, 2001.
13. Di Giorgio FP, Carrasco MA, Siao MC, Maniatis T, Eggan K. Non-cell autonomous effect of glia on motor neurons in an embryonic stem cell-based ALS model. Nat Neurosci 10: 608-614, 2007.
14. El Manira A, Kyriakatos A, Nanou E, Mahmood R. Endocannabinoid signaling in the spinal locomotor circuitry. Brain Res Rev 57: 29-36, 208.
15. Fellin T, Halassa MM, Terunuma M, Succol F, Takano H, Frank M, Moss SJ, Haydon PG. Endogenous nonneuronal modulators of synaptic transmission control cortical slow oscillations in vivo. Proc Natl Acad Sci U S A 106: 15037-15042, 2009.
16. Fonnum F, Johnsen A, Hassel B. Use of fluorocitrate and fluoroacetate in the study of brain metabolism. Glia 21: 106-113, 1997.
17. Funk GD, Kanjhan R, Walsh C, Lipski J, Comer AM, Parkis MA, Housley GD. P2 receptor excitation of rodent hypoglossal motoneuron activity in vitro and in vivo: a molecular physiological analysis. J Neurosci 17: 6325-6337, 1997.
18. Gosgnach S, Lanuza GM, Butt SJ, Saueressig H, Zhang Y, Velasquez T, Riethmacher D, Callaway EM, Kiehn O, Goulding M. V1 spinal neurons regulate the speed of vertebrate locomotor outputs. Nature 440: 215-219, 2006.
19. Goulding M. Circuits controlling vertebrate locomotion: moving in a new direction. Nat Rev Neurosci 10: 507-518, 2009.
20. Gourine AV, Kasymov V, Marina N, Tang F, Figueiredo MF, Lane S, Teschemacher AG, Spyer KM, Deisseroth K, Kasparov S. Astrocytes control breathing through pH-dependent release of ATP. Science 329: 571-575, 2010.
21. Grillner S. Biological pattern generation: the cellular and computational logic of networks in motion. Neuron 52: 751-766, 2006.
22. Halassa MM, Fellin T, Haydon PG. Tripartite synapses: roles for astrocytic purines in the control of synaptic physiology and behavior. Neuropharmacology 57: 343-346, 2009.
23. Hamilton NB, Attwell D. Do astrocytes really exocytose neurotransmitters? Nat Rev Neurosci 11: 227-238, 2010.
24. Hassel B, Paulsen RE, Johnsen A, Fonnum F. Selective inhibition of glial cell metabolism in vivo by fluorocitrate. Brain Res 576: 120-124, 1992.
25. Heckman CJ, Mottram C, Quinlan K, Theiss R, Schuster J. Motoneuron excitability: the importance of neuromodulatory inputs. Clin Neurophysiol 120: 2040-2054, 2009.
26. Herlenius E, Lagercrantz H. Adenosinergic modulation of respiratory neurons in the neonatal rat brainstem in vitro. J Physiol 518: 159-172, 1999.
27. Hülsmann S, Oku Y, Zhang W, Richter DW. Metabolic coupling between glia and neurons is necessary for maintaining respiratory activity in transverse medullary slices of neonatal mouse. Eur J Neurosci 12: 856-862, 2000.
28. Huxtable AG, Zwicker JD, Alvares TS, Ruangkittisakul A, Fang X, Hahn LB, Posse de Chaves E, Baker GB, Ballanyi K, Funk GD. Glia contribute to the purinergic modulation of inspiratory rhythm-generating networks. J Neurosci 30: 3947-3958, 2010.
29. Huxtable AG, Zwicker JD, Poon BY, Pagliardini S, Vrouwe SQ, Greer JJ, Funk GD. Tripartite purinergic modulation of central respiratory networks during perinatal development: the influence of ATP, ectonucleotidases, and ATP metabolites. J Neurosci 29: 14713-14725, 2009.
30. Jiang Z, Carlin KP, Brownstone RM. An in vitro functionally mature mouse spinal cord preparation for the study of spinal motor networks. Brain Res 816: 493-499, 1999.
31. Katz PS, Frost WN. Intrinsic neuromodulation: altering neuronal circuits from within. Trends Neurosci 19: 54-61, 1996.
32. Kawai A, Okada Y, Muckenhoff K, Scheid P. Theophylline and hypoxic ventilatory response in the rat isolated brainstem-spinal cord. Respir Physiol 100: 25-32, 1995.
33. Khawaled R, Bruening-Wright A, Adelman JP, Maylie J. Bicuculline block of small-conductance calcium-activated potassium channels. Pflügers Arch 438: 314-321, 1999.
34. Kiehn O. Locomotor circuits in the mammalian spinal cord. Annu Rev Neurosci 29: 279-306, 2006.
35. Kiehn O, Dougherty KJ, Hagglund M, Borgius L, Talpalar A, Restrepo CE. Probing spinal circuits controlling walking in mammals. Biochem Biophys Res Commun 396: 11-18, 2010.
36. Kjaerulff O, Kiehn O. Distribution of networks generating and coordinating locomotor activity in the neonatal rat spinal cord in vitro: a lesion study. J Neurosci 16: 5777-5794, 1996.
37. Largo C, Ibarz JM, Herreras O. Effects of the gliotoxin fluorocitrate on spreading depression and glial membrane potential in rat brain in situ. J Neurophysiol 78: 295-307, 1997.
38. Lorier AR, Huxtable AG, Robinson DM, Lipski J, Housley GD, Funk GD. P2Y1 receptor modulation of the pre-Botzinger complex inspiratory rhythm generating network in vitro. J Neurosci 27: 993-1005, 2007.
39. Miles GB, Hartley R, Todd AJ, Brownstone RM. Spinal cholinergic interneurons regulate the excitability of motoneurons during locomotion. Proc Natl Acad Sci U S A 104: 2448-2453, 2007.
40. Miles GB, Parkis MA, Lipski J, Funk GD. Modulation of phrenic motoneuron excitability by ATP: consequences for respiratory-related output in vitro. J Appl Physiol 92: 1899-1910, 2002.
41. Mironov SL, Langohr K, Richter DW. A1 adenosine receptors modulate respiratory activity of the neonatal mouse via the cAMP-mediated signaling pathway. J Neurophysiol 81: 247-255, 1999.
42. Munakata M, Akaike N. Theophylline affects three different potassium currents in dissociated rat cortical neurons. J Physiol 471: 599-616, 1993.
43. Mynlieff M, Beam KG. Adenosine acting at an A1 receptor decreases N-type calcium current in mouse motoneurons. J Neurosci 14: 3628-3634, 1994.
44. Nagai M, Re DB, Nagata T, Chalazonitis A, Jessell TM, Wichterle H, Przedborski S. Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons. Nat Neurosci 10: 615-622, 2007.
45. Newman EA. Glial cell inhibition of neurons by release of ATP. J Neurosci 23: 1659-1666, 2003.
46. Pascual O, Casper KB, Kubera C, Zhang J, Revilla-Sanchez R, Sul JY, Takano H, Moss SJ, McCarthy K, Haydon PG. Astrocytic purinergic signaling coordinates synaptic networks. Science 310: 113-116, 2005.
47. Pastor A, Chvátal A, Syková E, Kettenmann H. Glycine- and GABAactivated currents in identified glial cells of the developing rat spinal cord slice. Eur J Neurosci 7: 1188-1198, 1995.
48. Pflieger J-F, Clarac F, Vinay L. Picrotoxin and bicuculline have different effects on lumbar spinal networks and motoneurons in the neonatal rat. Brain Res 935: 81-86, 2002.
49. Rekling JC, Funk GD, Bayliss DA, Dong XW, Feldman JL. Synaptic control of motoneuronal excitability. Physiol Rev 80: 767-852, 2000.
50. Ronzio RA, Rowe WB, Meister A. Mechanism of inhibition of glutamine synthetase by methionine sulfoximine. Biochemistry 8: 1066-1075, 1969.
51. Schmidt C, Bellingham MC, Richter DW. Adenosinergic modulation of respiratory neurones and hypoxic responses in the anaesthetized cat. J Physiol 483: 769-781, 1995.
52. Serrano A, Haddjeri N, Lacaille JC, Robitaille R. GABAergic network activation of glial cells underlies hippocampal heterosynaptic depression. J Neurosci 26: 5370-5382, 2006.
53. Taccola G, Marchetti C, Nistri A. Modulation of rhythmic patterns and cumulative depolarization by group I metabotropic glutamate receptors in the neonatal rat spinal cord in vitro. Eur J Neurosci 19: 533-541, 2004.
54. Wall M, Dale N. Activity-dependent release of adenosine: a critical reevaluationof mechanism. Curr Neuropharm 6: 329-337, 2008.
55. Young JK, Dreshaj IA, Wilson CG, Martin RJ, Zaidi SIA, Haxhiu MA. An astrocyte toxin influences the pattern of breathing and the ventilatory response to hypercapnia in neonatal rats. Respir Physiol Neurobiol 147: 19-30, 2005.
56. Zagoraiou L, Akay T, Martin JF, Brownstone RM, Jessell TM, Miles GB. A cluster of cholinergic premotor interneurons modulates mouse locomotor activity. Neuron 64: 645-662, 2009.
57. Zhang JM, Wang HK, Ye CQ, Ge W, Chen Y, Jiang ZL, Wu CP, Poo MM, Duan S. ATP released by astrocytes mediates glutamatergic activitydependent heterosynaptic suppression. Neuron 40: 971-982, 2003.
58. Zwicker JD, Rajani V, Hahn LB, Funk GD. Purinergic modulation of preBotzinger complex inspiratory rhythm in rodents: the interaction between ATP and adenosine. J Physiol 589: 4583-4600, 2011.