Control of breathing by "nerve glue"

Science Signaling

Volumn 3, Issue 147, 2010, Pages

  Ballanyi, Klaus ^a   Panaitescu, Bogdan ^a   Ruangkittisakul, Araya ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM ION; GLUTAMIC ACID;

ASTROCYTE; BRAIN REGION; BRAIN STEM; BREATHING PATTERN; CEREBROSPINAL FLUID; CONTROLLED STUDY; GLIA; NERVE CELL; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NEUROTRANSMISSION; NONHUMAN; PRE BOTZINGER COMPLEX; PRIORITY JOURNAL; REVIEW; ARTICLE; BRAIN; BREATHING MECHANICS; HUMAN; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ADENOSINE TRIPHOSPHATE; BRAIN; GLUTAMIC ACID; HUMANS; NEUROGLIA; NEURONS; RESPIRATORY MECHANICS; SIGNAL TRANSDUCTION;

EID: 78149482560     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.3147pe41     Document Type: Review

References (36)

1. C. Iadecola, M. Nedergaard, Glial regulation of the cerebral microvasculature. Nat. Neurosci. 10, 1369-1376 (2007).
2. C. Agulhon, J. Petravicz, A. B. McMullen, E. J. Sweger, S. K. Minton, S. R. Taves, K. B. Casper, T. A. Fiacco, K. D. McCarthy, What is the role of astrocyte calcium in neurophysiology? Neuron 59, 932-946 (2008).
3. M. M. Halassa, P. G. Haydon, Integrated brain circuits: Astrocytic networks modulate neuronal activity and behavior. Annu. Rev. Physiol. 72, 335-355 (2010).
4. M. C. Morris, Fluorescent biosensors of intracellular targets from genetically encoded reporters to modular polypeptide probes. Cell Biochem. Biophys. 56, 19-37 (2010).
5. P. A. Gray, Transcription factors and the genetic organization of brain stem respiratory neurons. J. Appl. Physiol. 104, 1513-1521 (2008).
6. A. Ruangkittisakul, Y. Okada, Y. Oku, N. Koshiya, K. Ballanyi, Fluorescence imaging of active respiratory networks. Respir. Physiol. Neurobiol. 168, 26-38 (2009).
7. A. V. Gourine, V. Kasymov, N. Marina, F. Tang, M. F. Figueiredo, S. Lane, A. G. Teschemacher, K. M. Spyer, K. Deisseroth, S. Kasparov, Astrocytes control breathing through pH-dependent release of ATP. Science 329, 571-575 (2010).
8. M. R. Hodges, G. B. Richerson, Medullary serotonin neurons and their roles in central respiratory chemoreception. Respir. Physiol. Neurobiol. 173, 256-263 (2010).
9. P. G. Guyenet, R. L. Stornetta, D. A. Bayliss, Central respiratory chemoreception. J. Comp. Neurol. 518, 3883-3906 (2010).
10. J. L. Feldman, C. A. Del Negro, Looking for inspiration: New perspectives on respiratory rhythm. Nat. Rev. Neurosci. 7, 232-241 (2006).
11. J. C. Smith, H. H. Ellenberger, K. Ballanyi, D. W. Richter, J. L. Feldman, Pre-Bötzinger complex: A brainstem region that may generate respiratory rhythm in mammals. Science 254, 726-729 (1991).
12. + chemoreception in the cat pre-Bötzinger complex in vivo. J. Appl. Physiol. 88, 1996-2007 (2000).
13. 2 and pH, and their role as chemostimulants in the isolated respiratory network of neonatal rats. J. Physiol. 499, 527-542 (1997).
14. N. A. Ritucci, J. S. Erlichman, J. C. Leiter, R. W. Putnam, Response of membrane potential and intracellular pH to hypercapnia in neurons and astrocytes from rat retrotrapezoid nucleus. Am. J. Physiol. Regul. Integr. Comp. Physiol. 289, R851-R861 (2005).
15. D. R. McCrimmon, G. S. Mitchell, J. L. Feldman, G. F. Alheid, in The Encyclopedia of Neuroscience, L. Squire, T. Albright, F. Bloom, F. Gage, N. Spitzer, Eds. (Elsevier Science, Amsterdam, 2009), pp. 79-89.
16. + on the membrane potential of silent cells in the ventral and dorsal surface layers of the rat medulla in vitro. Pflügers Arch. 376, 229-235 (1978).
17. P. A. Gray, W. A. Janczewski, N. Mellen, D. R. McCrimmon, J. L. Feldman, Normal breathing requires pre-Bötzinger complex neurokinin-1 receptor-expressing neurons. Nat. Neurosci. 4, 927-930 (2001).
18. J. Bouvier, M. Thoby-Brisson, N. Renier, V. Dubreuil, J. Ericson, J. Champagnat, A. Pierani, A. Chédotal, G. Fortin, Hindbrain interneurons and axon guidance signaling critical for breathing. Nat. Neurosci. 13, 1066-1074 (2010).
19. K. Ballanyi, A. Ruangkittisakul, Structure-function analysis of rhythmogenic inspiratory pre-Bötzinger complex networks in "calibrated" newborn rat brainstem slices. Respir. Physiol. Neurobiol. 168, 158-178 (2009).
20. A. Ruangkittisakul, S. W. Schwarzacher, L. Secchia, Y. Ma, N. Bobocea, B. Y. Poon, G. D. Funk, K. Ballanyi, Generation of eupnea and sighs by a spatiochemically organized inspiratory network. J. Neurosci. 28, 2447-2458 (2008).
21. S. Hülsmann, Y. Oku, W. Zhang, D. W. Richter, 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).
22. A. G. Huxtable, J. D. Zwicker, T. S. Alvares, A. Ruangkittisakul, X. Fang, L. B. Hahn, E. Posse de Chaves, G. B. Baker, K. Ballanyi, G. D. Funk, Glia contribute to the purinergic modulation of inspiratory rhythm-generating networks. J. Neurosci. 30, 3947-3958 (2010).
23. G. D. Funk, A.G. Huxtable, A.R. Lorier, ATP in central respiratory control: A three-part signaling system. Respir. Physiol. Neurobiol. 164, 131-142 (2008).
24. R. W. Pace, C. A. Del Negro, AMPA and metabotropic glutamate receptors cooperatively generate inspiratory-like depolarization in mouse respiratory neurons in vitro. Eur. J. Neurosci. 28, 2434-2442 (2008).
25. K. Härtel, C. Schnell, S. Hülsmann, Astrocytic calcium signals induced by neuromodulators via functional metabotropic receptors in the ventral respiratory group of neonatal mice. Glia 57, 815-827 (2009).
26. D. Grass, P. G. Pawlowski, J. Hirrlinger, N. Papadopoulos, D. W. Richter, F. Kirchhoff, S. Hülsmann, Diversity of functional astroglial properties in the respiratory network. J. Neurosci. 24, 1358-1365 (2004).
27. S. Kuwana, N. Tsunekawa, Y. Yanagawa, Y. Okada, J. Kuribayashi, K. Obata, Electrophysiological and morphological characteristics of GABAergic respiratory neurons in the mouse pre-Bötzinger complex. Eur. J. Neurosci. 23, 667-674 (2006).
28. S. M. Winter, J. Hirrlinger, F. Kirchhoff, S. Hülsmann, Transgenic expression of fluorescent proteins in respiratory neurons. Respir. Physiol. Neurobiol. 159, 108-114 (2007).
29. N. Koshiya, J. C. Smith, Neuronal pacemaker for breathing visualized in vitro. Nature 400, 360-363 (1999).
30. J. A. Hayes, C. A. Del Negro, Neurokinin receptor-expressing pre-botzinger complex neurons in neonatal mice studied in vitro. J. Neurophysiol. 97, 4215-4224 (2007).
31. R. L. Stornetta, Identification of neurotransmitters and co-localization of transmitters in brainstem respiratory neurons. Respir. Physiol. Neurobiol. 164, 18-27 (2008).
32. E. D. Milligan, L. R. Watkins, Pathological and protective roles of glia in chronic pain. Nat. Rev. Neurosci. 10, 23-36 (2009).
33. E. E. Benarroch, Central neuron-glia interactions and neuropathic pain: Overview of recent concepts and clinical implications. Neurology 75, 273-278 (2010).
34. J. Bouvier, S. Autran, N. Dehorter, D. M. Katz, J. Champagnat, G. Fortin, M. Thoby-Brisson, Brain-derived neurotrophic factor enhances fetal respiratory rhythm frequency in the mouse pre-Bötzinger complex in vitro. Eur. J. Neurosci. 28, 510-520 (2008).
35. V. B. Lu, J. E. Biggs, M. J. Stebbing, S. Balasubramanyan, K. G. Todd, A. Y. Lai, W. F. Colmers, D. Dawbarn, K. Ballanyi, P. A. Smith, Brain-derived neurotrophic factor drives the changes in excitatory synaptic transmission in the rat superficial dorsal horn that follow sciatic nerve injury. J. Physiol. 587, 1013-1032 (2009).
36. Funding: This work was supported by the Canadian Institutes of Health Research (CIHR), the Alberta Heritage Foundation for Medical Research (AHFMR), and the Canada Foundation for Innovation (CFI-ASRIP). Acknowledgments: We are grateful for very helpful suggestions on earlier versions of the manuscript by G. F. Alheid and D. R. McCrimmon.