A quantitative model of cortical spreading depression due to purinergic and gap-junction transmission in astrocyte networks

Biophysical Journal

Volumn 95, Issue 12, 2008, Pages 5648-5660

  Bennett, Max R ^a   Farnell, Les ^a   Gibson, William G ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

PURINERGIC RECEPTOR;

ARTICLE; ASTROCYTE; BIOLOGICAL MODEL; CELL JUNCTION; CYTOLOGY; HIPPOCAMPUS; METABOLISM; NEOCORTEX; PHYSIOLOGY; SPINAL CORD; SPREADING CORTICAL DEPRESSION;

ASTROCYTES; GAP JUNCTIONS; HIPPOCAMPUS; MODELS, BIOLOGICAL; NEOCORTEX; RECEPTORS, PURINERGIC; SPINAL CORD; SPREADING CORTICAL DEPRESSION;

EID: 58749095320     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.108.137190     Document Type: Article

References (48)

1. Leao, A. A. P. 1944. Spreading depression of activity in the cerebral cortex. J. Neurophysiol. 7:359-390.
2. Leao, A. A. 1951. The slow voltage variation of cortical spreading depression of activity. Electroencephalogr. Clin. Neurophysiol. 3:315-321.
3. Somjen, G. G. 2001. Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. Physiol. Rev. 81:1065-1096.
4. Kunkler, P. E., R. E. Hulse, M. W. Schmitt, C. Nicholson, and R. P. Kraig. 2005. Optical current source density analysis in hippocampal organotypic culture shows that spreading depression occurs with uniquely reversing currents. J. Neurosci. 25:3952-3961.
5. Kruger, H., U. Heinemann, and H. J. Luhmann. 1999. Effects of ionotropic glutamate receptor blockade and 5-HT1A receptor activation on spreading depression in rat neocortical slices. Neuroreport. 10:2651-2656.
6. Martins-Ferreira, H., M. Nedergaard, and C. Nicholson. 2000. Perspectives on spreading depression. Brain Res. Brain Res. Rev. 32:215-234.
7. Anderson, T., and R. Andrew. 2002. Spreading depression: imaging and blockade in the rat neocortical brain slice. J. Neurophysiol. 88:2713-2725.
8. 2+ waves and spreading depression in the mouse neocortex. J. Neurosci. 23:9888-9896.
9. Bowser, D. N., and B. S. Khakh. 2007. Vesicular ATP is the predominant cause of intercellular calcium waves in astrocytes. J. Gen. Physiol. 129:485-491.
10. Schock, S. C., N. Munyao, Y. Yakubchyk, L. A. Sabourin, A. M. Hakim, E. C. G. Ventureyra, and C. S. Thompson. 2007. Cortical spreading depression releases ATP into the extracellular space and purinergic receptor activation contributes to the induction of ischemic tolerance. Brain Res. 1168:129-138.
11. Basarsky, T. A., S. Duffy, R. D. Andrew, and B. A. MacVicar. 1998. Imaging spreading depression and associated calcium dynamics in brain slices. J. Neurosci. 18:7189-7199.
12. Chuquet, J., L. Hollander, and E. A. Nimchinsky. 2007. High-resolution in vivo imaging of the neurovascular unit during spreading depression. J. Neurosci. 27:4036-4044.
13. Rao, S. P., and S. K. Sidar. 2006. Astrocytes in 17b-estradiol treated mixed hippocampal cultures show attenuated calcium response to neuronal activity. Glia. 53:817-826.
14. Takano, T., J. Kang, J. K. Jaiswal, S. M. Simon, J. H. C. Lin, Y. Yu, Y. Li, J. Yang, G. Dienel, H. R. Zielke, et al. 2005. Receptor-mediated glutamate release from volume sensitive channels in astrocytes. Proc. Natl. Acad. Sci. USA. 102:16466-16471.
15. Shiga, H., J. Murakami, T. Nagao, M. Tanaka, K. Kawahara, I. Matsuoka, and E. Ito. 2006. Glutamate release from astrocytes is stimulated via the appearance of exocytosis during cyclic AMP-induced morphologic changes. J. Neurosci. Res. 84:338-347.
16. Fellin, T., T. Pozzan, and G. Carmignoto. 2006. Purinergic receptors mediate two distinct glutamate release pathways in hippocampal astrocytes. J. Biol. Chem. 281:4274-4284.
17. Coco, S., F. Calegari, E. Pravettoni, D. Pozzi, E. Taverna, P. Rosa, M. Matteoli, and C. Verderio. 2003. Storage and release of ATP from astrocytes in culture. J. Biol. Chem. 278:1354-1362.
18. Werry, E. L., G. J. Liu, and M. R. Bennett. 2006. Glutamate-stimulated ATP release from spinal cord astrocytes is potentiated by substance P. J. Neurochem. 99:924-936.
19. Robert, A., J. A. Black, and S. G. Waxman. 1998. Endogenous NMDA-receptor activation regulates glutamate release in cultured spinal neurons. J. Neurophysiol. 80:196-208.
20. Monyer, H., R. Sprengel, R. Schoepfer, A. Herb, M. Higuchi, H. Lomeli, N. Burnashev, B. Sakmann, and P. Seeburg. 1992. Heteromeric NMDA receptors: Molecular and functional distinction of subtypes. Science. 256:1217-1221.
21. Binshtok, A. M., I. A. Fleidervish, R. Sprengel, and M. J. Gutnick. 2006. NMDA receptors in layer 4 spiny stellate cells of the mouse barrel cortex contain the NR2C subunit. J. Neurosci. 26:708-715.
22. Queiroz, G., D. K. Meyer, A. Meyer, K. Starke, and I. von Kugelgen. 1999. A study of the mechanism of the release of ATP from rat cortical astroglial cells evoked by activation of glutamate receptors. Neuroscience. 91:1171-1181.
23. Vesce, S., D. Rossi, L. Brambilla, and A. Volterra. 2007. Glutamate release from astrocytes in physiological conditions and in neurodegenerative disorders characterized by neuroinflammation. Int. Rev. Neurobiol. 82:57-71.
24. Halassa, M. M., T. Fellin, and P. G. Haydon. 2007. The tripartite synapse: roles for gliotransmission in health and disease. Trends Mol. Med. 13:54-63.
25. + channels in rat hippocampal astrocytes. J. Neurosci. 23:1678-1687.
26. Gallagher, C. J., and M. W. Salter. 2003. Differential properties of astrocyte calcium waves mediated by P2Y1 and P2Y2 receptors. J. Neurosci. 23:6728-6739.
27. Theis, M., R. Jauch, L. Zhuo, D. Speidel, A. Wallraff, B. Döring, C. Frisch, G. Söhl, B. Teubner, C. Euwens, et al. 2003. Accelerated hippocampal spreading depression and enhanced locomotory activity in mice with astrocyte-directed inactivation of connexin43. J. Neurosci. 23:766-776.
28. Haas, B., C. G. Schipke, O. Peters, G. Söhl, K. Willecke, and H. Kettenmann. 2006. Activity-dependent ATP-waves in the mouse neocortex are independent from astrocytic calcium waves. Cereb. Cortex. 16:237-246.
29. Bennett, M. R., L. Farnell, and W. G. Gibson. 2005. A quantitative model of purinergic junctional transmission of calcium waves in astrocyte networks. Biophys. J. 89:2235-2250.
30. Bennett, M. R., V. Buljan, L. Farnell, and W. G. Gibson. 2006. Purinergic junctional transmission and propagation of calcium waves in spinal cord astrocyte networks. Biophys. J. 91:3560-3571.
31. Montana, V., E. Malarkey, C. Verderio, M. Matteoli, and V. Parpura. 2006. Vesicular transmitter release from astrocytes. Glia. 54:700-715.
32. Jourdain, P., L. H. Bergersen, K. Bhaukaurally, P. Bezzi, M. Santello, M. Domercq, C. Matute, F. Tonello, V. Gundersen, and A. Volterra. 2007. Glutamate exocytosis from astrocytes controls synaptic strength. Nat. Neurosci. 10:331-339.
33. Magistretti, P., and L. Pellerin. 1999. Cellular mechanisms of brain energy metabolism and their relevance to functional brain imaging. Philos. Trans. R. Soc. Lond. B Biol. Sci. 354:1155-1163.
34. Reference deleted in proof.
35. Domercq, M., L. Brambilla, E. Pilati, J. Marchaland, A. Volterra, and P. Bezzi. 2006. P2Y1 receptor-evoked glutamate exocytosis from astrocytes. J. Biol. Chem. 281:30684-30696.
36. Destexhe, A., Z. F. Mainen, and T. J. Sejnowski. 1994. Synthesis of models for excitable membranes, synaptic transmission and neuromodulation using a common kinetic formalism. J. Comp. Neurol. 1:195-230.
37. Hofer, T., L. Venance, and C. Giaume. 2002. Control and plasticity of intercellular calcium waves in astrocytes: a modeling approach. J. Neurosci. 22:4850-4859.
38. Makarova, J., J. M. Ibarz, S. Canals, and O. Herreras. 2007. A steady-state model of spreading depression predicts the importance of an unknown conductance in specific dendritic domains. Biophys. J. 92:4216-4232.
39. Almeida, A. C., H. Z. Texeira, M. A. Duarte, and A. F. Infantosi. 2004. Modeling extracellular space electrodiffusion during Leao's spreading depression. IEEE Trans. Biomed. Eng. 51:450-458.
40. Higashida, H., G. Mitarai, and S. Watanabe. 1974. A comparative study of membrane potential changes in neurons and neuroglial cells during spreading depression in the rabbit. Brain Res. 65:411-425.
41. Sugaya, E., M. Takato, and Y. Noda. 1975. Neuronal and glial activity during spreading depression in cerebral cortex of cat. J. Neurophysiol. 38:822-841.
42. Somjen, G. G. 2004. Ions in the Brain. Oxford, New York.
43. Largo, C., J. M. Ibarz, and O. Herreras. 1997. Effects of the gliotoxin fluorocitrate on spreading depression and glial membrane potential in rat brain in situ. J. Neurophysiol. 78:295-307.
44. 2+ signaling. J. Neurosci. 26:1378-1385.
45. Shapiro, B. E. 2001. Osmotic forces and gap junctions in spreading depression: a computational model. J. Comput. Neurosci. 10:99-120.
46. Smith, J. M., D. P. Bradley, M. F. James, and C. L. H. Huang. 2006. Physiological studies of cortical spreading depression. Biol. Rev. Camb. Philos. Soc. 81:457-481.
47. Teixeira, H. Z., A. C. G. Almeida, A. F. C. Infantosi, M. A. Vasconcelos, and M. A. Duarte. 2004. Simulation of the effect of Na and Cl on the velocity of a spreading depression wave using a simplified electrochemical model of synaptic terminals. J. Neural Eng. 1:117-126.
48. Hille, B. 1992. Ionic Channels of Excitable Membranes. Sinauer, Sunderland, MA.