Neuroglial ATP release through innexin channels controls microglial cell movement to a nerve injury

Journal of General Physiology

Volumn 136, Issue 4, 2010, Pages 425-442

  Samuels, Stuart E ^a   Lipitz, Jeffrey B ^a   Dahl, Gerhard ^a   Muller, Kenneth J ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; GAP JUNCTION PROTEIN;

ANIMAL; ARTICLE; CALCIUM SIGNALING; CELL MOTION; GENETICS; GLIA; LEECH; METABOLISM; MICROGLIA; NERVE CRUSH; NERVOUS SYSTEM INJURY; OOCYTE; PHYSIOLOGY; RNA INTERFERENCE; XENOPUS;

ADENOSINE TRIPHOSPHATE; ANIMALS; CALCIUM SIGNALING; CELL MOVEMENT; CONNEXINS; LEECHES; MICROGLIA; NERVE CRUSH; NEUROGLIA; OOCYTES; RNA INTERFERENCE; TRAUMA, NERVOUS SYSTEM; XENOPUS;

EID: 77957834139     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.201010476     Document Type: Article

References (108)

1. Abbracchio, M.P., and C. Verderio. 2006. Pathophysiological roles of P2 receptors in glial cells. Novartis Found. Symp. 276:91-103. doi:10.1002/ 9780470032244.ch8
2. Anderson, C.M., J.P. Bergher, and R.A. Swanson. 2004. ATP-induced ATP release from astrocytes. J. Neurochem. 88:246-256. doi:10.1111/j.1471-4159.2004. 02204.x
3. Babington, E.J., J. Vatanparast, J. Verrall, and S.E. Blackshaw. 2005. Three-dimensional culture of leech and snail ganglia for studies of neural repair. Invert. Neurosci. 5:173-182. doi:10 .1007/s10158-005-0006-7
4. Baker, M.W., and E.R. Macagno. 2000. RNAi of the receptor tyrosine phosphatase HmLAR2 in a single cell of an intact leech embryo leads to growth-cone collapse. Curr. Biol. 10:1071-1074. doi:10.1016/S0960-9822(00)00674- 6
5. Bao, L., S. Locovei, and G. Dahl. 2004. Pannexin membrane channels are mechanosensitive conduits for ATP. FEBS Lett. 572:65-68. doi:10.1016/j.febslet. 2004.07.009 (Pubitemid 39092514)
6. Bao, L., S. Samuels, S. Locovei, E.R. Macagno, K.J. Muller, and G. Dahl. 2007. Innexins form two types of channels. FEBS Lett. 581:5703-5708. doi:10.1016/j.febslet.2007.11.030 (Pubitemid 350179781)
7. Barbe, M.T., H. Monyer, and R. Bruzzone. 2006. Cell-cell communication beyond connexins: the pannexin channels. Physiology (Bethesda). 21:103-114.
8. Bianco, F., M. Fumagalli, E. Pravettoni, N. D'Ambrosi, C. Volonte, M. Matteoli, M.P. Abbracchio, and C. Verderio. 2005a. Pathophysiological roles of extracellular nucleotides in glial cells: differential expression of purinergic receptors in resting and activated microglia. Brain Res. Brain Res. Rev. 48:144-156.doi:10.1016/j.brainresrev.2004.12.004 (Pubitemid 40585745)
9. Bianco, F., E. Pravettoni, A. Colombo, U. Schenk, T. Möller, M. Matteoli, and C. Verderio. 2005b. Astrocyte-derived ATP induces vesicle shedding and IL-1 beta release from microglia. J. Immunol. 174:7268-7277.
10. 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. doi:10.1085/jgp.200709780 (Pubitemid 46849148)
11. Brown, C., Y Lin, and A. Hassid. 2001. Requirement of protein tyrosine phosphatase SHP2 for NO-stimulated vascular smooth muscle cell motility. Am. J. Physiol. Heart Circ. Physiol. 281:H1598-H1605.
12. Bruzzone, R., M.T. Barbe, N.J. Jakob, and H. Monyer. 2005. Pharmacological properties of homomeric and heteromeric pannexin hemichannels expressed in Xenopus oocytes. J. Neurochem. 92:1033-1043. doi:10.1111/j.1471- 4159.2004.02947.x (Pubitemid 40344294)
13. Bulotta, S., M.V. Ierardi, J. Maiuolo, M.G. Cattaneo, A. Cerullo, L.M. Vicentini, and N. Borgese. 2009. Basal nitric oxide release attenuates cell migration of HeLa and endothelial cells. Biochem. Biophys. Res. Commun. 386:744-749. doi:10.1016/j.bbrc.2009.06.118
14. Chen, A., S.M. Kumar, C.L. Sahley, and K.J. Muller. 2000. Nitric oxide influences injury-induced microglial migration and accumulation in the leech CNS. J. Neurosci. 20:1036-1043.
15. Chen, T., K. Koga, X.Y. Li, and M. Zhuo. 2010. Spinal microglial motility is independent of neuronal activity and plasticity in adult mice. Mol. Pain. 6:19. doi:10.1186/1744-8069-6-19
16. Chen, Y., R. Corriden, Y Inoue, L. Yip, N. Hashiguchi, A. Zinkernagel, V. Nizet, RA. Insel, and W.G. Junger. 2006. ATP release guides neutrophil chemotaxis via P2Y2 and A3 receptors. Science. 314:1792-1795. doi:10.1126/science.1132559 (Pubitemid 44969094)
17. Choi, M.S., K.S. Cho, S.M. Shin, H.M. Ko, K.J. Kwon, C.Y. Shin, and K.H. Ko. 2010. ATP induced microglial cell migration through non-transcriptional activation of matrix metalloproteinase-9. Arch. Pharm. Res. 33:257-265. doi:10.1007/s12272-010-0211-8
18. Coggeshall, R.E., and D.W. Fawcett. 1964. The fine structure of the central nervous system of the leech, Hirudo medicinalis. J. Neurophysiol. 27:229-289.
19. Cotrina, M.L., J.H. Lin, A. Alves-Rodrigues, S. Liu, J. Li, H. Azmi- Ghadimi, J. Kang, C.C. Naus, and M. Nedergaard. 1998a. Connexins regulate calcium signaling by controlling ATP release. Proc. Natl. Acad. Sci. USA. 95:15735-15740. doi:10.1073/pnas.95.26.15735 (Pubitemid 29018769)
20. Cotrina, M.L., J.H. Lin, and M. Nedergaard. 1998b. Cytoskeletal assembly and ATP release regulate astrocytic calcium signaling. J. Neurosci. 18:8794-8804. (Pubitemid 28491745)
21. Cotrina, M.L., J.H. Lin, J.C. López-García, C.C. Naus, and M. Nedergaard. 2000. ATP-mediated glia signaling. J. Neurosci. 20:2835-2844.
22. Coutinho-Silva, R., G. Corrêa, A.A. Sater, and D.M. Ojcius. 2009. The P2X7 receptor and intracellular pathogens: a continuing struggle. Purinergic Signal. 5:197-204. doi:10.1007/s11302-009-9130-x
23. Dahl, G., and S. Locovei. 2006. Pannexin: to gap or not to gap, is that a question? IUBMB Life. 58:409-419. doi:10.1080/15216540600794526 (Pubitemid 43995626)
24. Davalos, D., J. Grutzendler, G. Yang, J.V. Kim, Y. Zuo, S. Jung, D.R. Littman, M.L. Dustin, and W.B. Gan. 2005. ATP mediates rapid microglial response to local brain injury in vivo. Nat. Neurosci. 8:752-758. doi:10.1038/nn1472 (Pubitemid 43085841)
25. Deitmer, J.W., C.R. Rose, T. Munsch, J. Schmidt, W. Nett, H.P. Schneider, and C. Lohr. 1999. Leech giant glial cell: functional role in a simple nervous system. Glia. 28:175-182. doi:10.1002/(SICI)1098-1136(199912)28:3<175::AID- GLIA1>3.0.CO;2-7
26. del Rio Hortega, P. 1920. La microglia y su transformacion celulas en basoncito y cuerpos granulo-adiposos. Trab. Lab. Invest. Biol. Univ. Madrid. 18:37-82.
27. del Rio Hortega, P. 1932. Microglia. In Cytology and Cellular Pathology of the Nervous System. W. Penfield, editor. Paul B. Hoeber, New York. 483-543.
28. Duan, Y., S.J. Haugabook, C.L. Sahley, and K.J. Muller. 2003. Methylene blue blocks cGMP production and disrupts directed migration of microglia to nerve lesions in the leech CNS. J. Neurobiol. 57:183-192. doi:10.1002/neu.10262 (Pubitemid 37280807)
29. Duan, Y., J. Panoff, B.D. Burrell, C.L. Sahley, and K.J. Muller. 2005. Repair and regeneration of functional synaptic connections: cellular and molecular interactions in the leech. Cell. Mol. Neurobiol. 25:441-450. doi:10.1007/s10571-005-3152-x (Pubitemid 40768444)
30. Duan, Y., C.L. Sahley, and K.J. Muller. 2009. ATP and NO dually control migration of microglia to nerve lesions. Dev. Neurobiol. 69:60-72. doi:10.1002/dneu.20689
31. Dykes, I.M., and E.R. Macagno. 2006. Molecular characterization and embryonic expression of innexins in the leech Hirudo medicinalis. Dev. Genes Evol. 216:185-197. doi:10.1007/s00427-005-0048-1
32. Elliot, E.J., and K.J. Muller. 1981. Long-term survival of glial segments during nerve regeneration in the leech. Brain Res. 218:99-113. doi:10.1016/0006-8993(81)90991-4 (Pubitemid 11083167)
33. Ferrari, D., S. Wesselborg, M.K. Bauer, and K. Schulze-Osthoff. 1997. Extracellular ATP activates transcription factor NF-kappaB through the P2Z purinoreceptor by selectively targeting NF-kappaB p65. J. Cell Biol. 139:1635-1643. doi:10.1083/jcb.139.7.1635 (Pubitemid 28079229)
34. Fiacco, T.A., and K.D. McCarthy. 2004. Intracellular astrocyte calcium waves in situ increase the frequency of spontaneous AMPA receptor currents in CA1 pyramidal neurons. J. Neurosci. 24:722-732. doi:10.1523/JNEUROSCI.2859-03. 2004 (Pubitemid 38166498)
35. Fleming, I., and R. Busse. 1999. Signal transduction of eNOS activation. Cardiovasc. Res. 43:532-541. doi:10.1016/S0008-6363(99)00094-2 (Pubitemid 29369252)
36. Floyd, C.L., B.A. Rzigalinski, J.T. Weber, H.A. Sitterding, K.A. Willoughby, and E.F. Ellis. 2001. Traumatic injury of cultured astrocytes alters inositol (1,4,5)-trisphosphate-mediated signaling. Glia. 33:12-23. doi:10.1002/1098-1136(20010101)33:1<12:: AID-GLIA1002>3.0.CO;2-V
37. Franchi, L., T. Eigenbrod, R. Muñoz-Planillo, and G. Nuñez. 2009. The inflammasome: a caspase-1-activation platform that regulates immune responses and disease pathogenesis. Nat. Immunol. 10:241-247. doi:10.1038/ni.1703
38. Gehrmann, J., Y. Matsumoto, and G.W. Kreutzberg. 1995. Microglia: intrinsic immuneffector cell of the brain. Brain Res. Brain Res. Rev. 20:269-287. doi:10.1016/0165-0173(94)00015-H
39. Gray, E.G., and R.W. Guillery. 1963. An electron microscopical study of the ventral nerve cord of the leech. Z. Zellforsch. Mikrosk. Anat. 60:826-849. doi:10.1007/BF00339095
40. Griffin, J.W., and W.J. Thompson. 2008. Biology and pathology of nonmyelinating Schwann cells. Glia. 56:1518-1531. doi:10.1002/glia.20778
41. Guthrie, P.B., J. Knappenberger, M. Segal, M.V. Bennett, A.C. Charles, and S.B. Kater. 1999. ATP released from astrocytes mediates glial calcium waves. J. Neurosci. 19:520-528.
42. Hassinger, T.D., P.B. Guthrie, P.B. Atkinson, M.V. Bennett, and S.B. Kater. 1996. An extracellular signaling component in propagation of astrocytic calcium waves. Proc. Natl. Acad. Sci. USA. 93:13268-13273. doi:10.1073/pnas.93. 23.13268 (Pubitemid 26382805)
43. Haynes, S.E., G. Hollopeter, G. Yang, D. Kurpius, M.E. Dailey, W.B. Gan, and D. Julius. 2006. The P2Y12 receptor regulates microglial activation by extracellular nucleotides. Nat. Neurosci. 9:1512-1519. doi:10.1038/nn1805 (Pubitemid 44862659)
44. Honda, S., Y. Sasaki, K. Ohsawa, Y. Imai, Y. Nakamura, K. Inoue, and S. Kohsaka. 2001. Extracellular ATP or ADP induce chemotaxis of cultured microglia through Gi/o-coupled P2Y receptors. J. Neurosci. 21:1975-1982.
45. Huang, Y., J.B. Grinspan, C.K. Abrams, and S.S. Scherer. 2007. Pannexin1 is expressed by neurons and glia but does not form functional gap junctions. Glia. 55:46-56. doi:10.1002/glia.20435 (Pubitemid 44845508)
46. Hubel, D.H. 1957. Tungsten microelectrode for recording from single units. Science. 125:549-550. doi:10.1126/science.125.3247.549
47. Iglesias, R., S. Locovei, A. Roque, A.P. Alberto, G. Dahl, D.C. Spray, and E. Scemes. 2008. P2X7 receptor-Pannexin1 complex: pharmacology and signaling. Am. J. Physiol. Cell Physiol. 295:C752-C760. doi:10.1152/ajpcell. 00228.2008
48. Iglesias, R., G. Dahl, F. Qiu, D.C. Spray, and E. Scemes. 2009. Pannexin 1: the molecular substrate of astrocyte "hemichannels". J. Neurosci. 29:7092-7097. doi:10.1523/JNEUROSCI.6062-08.2009
49. Inoue, K. 2002. Microglial activation by purines and pyrimidines. Glia. 40:156-163. doi:10.1002/glia.10150 (Pubitemid 35337373)
50. James, G., and A.M. Butt. 2002. P2Y and P2X purinoceptor mediated Ca2+ signalling in glial cell pathology in the central nervous system. Eur. J. Pharmacol. 447:247-260. doi:10.1016/S0014-2999(02)01756-9. (Pubitemid 34874458)
51. Kai-Kai, M.A., and V.W. Pentreath. 1981. The structure, distribution, and quantitative relationships of the glia in the abdominal ganglia of the horse leech, Haemopis sanguisuga. J. Comp. Neurol. 202:193-210. doi:10.1002/cne. 902020206 (Pubitemid 11027956)
52. Kanneganti, T.D., M. Lamkanfi, Y.G. Kim, G. Chen, J.H. Park, L. Franchi, P. Vandenabeele, and G. Núñez. 2007. Pannexin-1- mediated recognition of bacterial molecules activates the cryopyrin inflammasome independent of Toll-like receptor signaling. Immunity. 26:433-443. doi:10.1016/j.immuni.2007.03.008 (Pubitemid 46603000)
53. Kennerdell, J.R., and R.W. Carthew. 1998. Use of dsRNA- mediated genetic interference to demonstrate that frizzled and frizzled 2 act in the wingless pathway. Cell. 95:1017-1026. doi:10.1016/S0092-8674(00)81725-0 (Pubitemid 29019053)
54. Kim, W.T., M.G. Rioult, and A.H. Cornell-Bell. 1994. Glutamateinduced calcium signaling in astrocytes. Glia. 11:173-184. doi:10.1002/glia.440110211
55. Kuffler, S.W., and J.G. Nicholls. 1966. The physiology of neuroglial cells. Ergeb. Physiol. 57:1-90.
56. Kuffler, S.W., and D.D. Potter. 1964. Glia in the leech central nervous system: physiological properties and neuron-glia relationship. J. Neurophysiol. 27:290-320.
57. Kumar, S.M., D.M. Porterfield, K.J. Muller, PJ. Smith, and C.L. Sahley. 2001. Nerve injury induces a rapid efflux of nitric oxide (NO) detected with a novel NO microsensor. J. Neurosci. 21:215-220.
58. Lamkanfi, M., T.D. Kanneganti, L. Franchi, and G. Núñez. 2007. Caspase-1 inflammasomes in infection and inflammation. J. Leukoc. Biol. 82:220-225. doi:10.1189/jlb.1206756 (Pubitemid 47230630)
59. Li, N., J.Y. Sul, and P.G. Haydon. 2003. A calcium-induced calcium influx factor, nitric oxide, modulates the refilling of calcium stores in astrocytes. J. Neurosci. 23:10302-10310.
60. Lipitz, J. 2008. Cannabanoids and the control of microglial migration. PhD thesis. University of Miami, Coral Gables, FL. 105 pp.
61. Locovei, S., L. Bao, and G. Dahl. 2006a. Pannexin 1 in erythrocytes: function without a gap. Proc. Natl. Acad. Sci. USA. 103:7655-7659. doi:10.1073/pnas.0601037103
62. Locovei, S., J. Wang, and G. Dahl. 2006b. Activation of pannexin 1 channels by ATP through P2Y receptors and by cytoplasmic calcium. FEBS Lett. 580:239-244. doi:10.1016/j.febslet.2005.12.004 (Pubitemid 43005343)
63. Locovei, S., E. Scemes, F. Qiu, D.C. Spray, and G. Dahl. 2007. Pannexin1 is part of the pore forming unit of the P2X(7) receptor death complex. FEBS Lett. 581:483-488. doi:10.1016/j.febslet.2006.12.056 (Pubitemid 46149626)
64. Lohr, C., and J.W. Deitmer. 1999. Dendritic calcium transients in the leech giant glial cell in situ. Glia. 26:109-118. doi:10.1002/ (SICI)1098-1136(199904)26:2<109::AID-GLIA2>3.0.CO;2-J
65. Lohr, C., and J.W. Deitmer. 2006. Calcium signaling in invertebrate glial cells. Glia. 54:642-649. doi:10.1002/glia.20368 (Pubitemid 44629627)
66. MacVicar, B.A., and R.J. Thompson. 2010. Non-junction functions of pannexin-1 channels. Trends Neurosci. 33:93-102. doi:10.1016/j.tins.2009.11.007
67. Masuda-Nakagawa, L.M., K.J. Muller, and J.G. Nicholls. 1990. Accumulation of laminin and microglial cells at sites of injury and regeneration in the central nervous system of the leech. Proc. Biol. Sci. 241:201-206. doi:10.1098/rspb.1990.0086
68. McGlade-McCulloh, E., A.M. Morrissey, F. Norona, and K.J. Muller. 1989. Individual microglia move rapidly and directly to nerve lesions in the leech central nervous system. Proc. Natl. Acad. Sci. USA. 86:1093-1097. doi:10.1073/pnas.86.3.1093 (Pubitemid 19056297)
69. Metea, M.R., and E.A. Newman. 2006. Calcium signaling in specialized glial cells. Glia. 54:650-655. doi:10.1002/glia.20352 (Pubitemid 44629628)
70. Mills, L.R., A.A. Velumian, S.K. Agrawal, E. Theriault, and M.G. Fehlings. 2004. Confocal imaging of changes in glial calcium dynamics and homeostasis after mechanical injury in rat spinal cord white matter. Neuroimage. 21:1069-1082. doi:10.1016/j.neuroimage.2003.10.041 (Pubitemid 38314970)
71. Morgese, V.J., E.J. Elliott, and K.J. Muller. 1983. Microglial movement to sites of nerve lesion in the leech CNS. Brain Res. 272:166-170. doi:10.1016/0006-8993(83)90375-X (Pubitemid 13076241)
72. Müller, M., A. Henrich, J. Klockenhoff, P.W. Dierkes, and W.R. Schlue. 2000. Effects of ATP and derivatives on neuropile glial cells of the leech central nervous system. Glia. 29:191-201. doi:10.1002/(SICI)1098- 1136(20000201)29:3<191::AID-GLIA1>3.0.CO;2-R
73. Newman, E.A. 2001. Propagation of intercellular calcium waves in retinal astrocytes and Müller cells. J. Neurosci. 21:2215-2223.
74. Ngu, E.M., C.L. Sahley, and K.J. Muller. 2007. Reduced axon sprouting after treatment that diminishes microglia accumulation at lesions in the leech CNS. J. Comp. Neurol. 503:101-109. doi:10.1002/cne.21386 (Pubitemid 47024420)
75. Nicholls, J.G., and D.E. Wolfe. 1967. Distribution of 14C-labeled sucrose, inulin, and dextran in extracellular spaces and in cells of the leech central nervous system. J. Neurophysiol. 30:1574-1592.
76. Nimmerjahn, A., F. Kirchhoff, and F. Helmchen. 2005. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science. 308:1314-1318. doi:10.1126/science.1110647 (Pubitemid 40746128)
77. Oland, L.A., J.P. Biebelhausen, and L.P. Tolbert. 2008. Glial investment of the adult and developing antennal lobe of Drosophila. J. Comp. Neurol. 509:526-550. doi:10.1002/cne.21762
78. Ostrow, L.W., and F. Sachs. 2005. Mechanosensation and endothelin in astrocytes-hypothetical roles in CNS pathophysiology. Brain Res. Brain Res. Rev. 48:488-508. doi:10.1016/j.brainresrev.2004.09.005 (Pubitemid 40725402)
79. Parri, H.R., and V. Crunelli. 2003. The role of Ca2+ in the generation of spontaneous astrocytic Ca2+ oscillations. Neuroscience. 120:979-992. doi:10.1016/S0306-4522(03)00379-8 (Pubitemid 36966650)
80. Pelegrin, P., and A. Surprenant. 2006. Pannexin-1 mediates large pore formation and interleukin-1beta release by the ATP-gated P2X7 receptor. EMBO J. 25:5071-5082. doi:10.1038/sj.emboj.7601378 (Pubitemid 44658525)
81. Pelegrin, P., C. Barroso-Gutierrez, and A. Surprenant. 2008. P2X7 receptor differentially couples to distinct release pathways for IL-1beta in mouse macrophage. J. Immunol. 180:7147-7157.
82. Ransford, G.A., N. Fregien, F. Qiu, G. Dahl, G.E. Conner, and M. Salathe. 2009. Pannexin 1 contributes to ATP release in airway epithelia. Am. J. Respir. Cell Mol. Biol. 41:525-534. doi:10.1165/rcmb.2008-0367OC
83. Ready, D.F., andJ. Nicholls. 1979. Identified neurones isolated from leech CNS make selective connections in culture. Nature. 281: 67-69. doi:10.1038/281067a0 (Pubitemid 9247993)
84. Rose, C.R., C. Lohr, and J.W. Deitmer. 1995. Activity-induced Ca2+ transients in nerve and glial cells in the leech CNS. Neuroreport. 6:642-644. doi:10.1097/00001756-199503000-00014
85. Salter, M.W., and J.L. Hicks. 1995. ATP causes release of intracellular Ca2+ via the phospholipase C beta/IP3 pathway in astrocytes from the dorsal spinal cord. J. Neurosci. 15:2961-2971.
86. Samuels, S.E. 2009. Innexons, membrane channels for ATP, control microglia migration to nerve lesions. PhD thesis. University of Miami, Coral Gables, FL. 108 pp.
87. Scemes, E., and C. Giaume. 2006. Astrocyte calcium waves: what they are and what they do. Glia. 54:716-725. doi:10.1002/glia.20374 (Pubitemid 44629634)
88. Scemes, E., S.O. Suadicani, G. Dahl, and D.C. Spray. 2007. Connexin and pannexin mediated cell-cell communication. Neuron Glia Biol. 3:199-208. doi:10.1017/S1740925X08000069 (Pubitemid 351594228)
89. Schipke, C.G., C. Boucsein, C. Ohlemeyer, F. Kirchhoff, and H. Kettenmann. 2002. Astrocyte Ca2+ waves trigger responses in microglial cells in brain slices. FASEB J. 16:255-257.
90. Shafer, O.T., A. Chen, S.M. Kumar, K.J. Muller, and C.L. Sahley. 1998. Injury-induced expression of endothelial nitric oxide synthase by glial and microglial cells in the leech central nervous system within minutes after injury. Proc. Biol. Sci. 265:2171-2175. doi:10.1098/rspb.1998.0555
91. Shao, Y., and K.D. McCarthy. 1995. Receptor-mediated calcium signals in astroglia: multiple receptors, common stores and allor-nothing responses. Cell Calcium. 17:187-196. doi:10.1016/0143-4160(95)90033-0
92. Silverman, W.R., J.P. de Rivero Vaccari, S. Locovei, F. Qiu, S.K. Carlsson, E. Scemes, R.W. Keane, and G. Dahl. 2009. The pannexin 1 channel activates the inflammasome in neurons and astrocytes. J. Biol. Chem. 284:18143-18151. doi:10.1074/jbc.M109.004804
93. Son, Y.J., J.T. Trachtenberg, and W.J. Thompson. 1996. Schwann cells induce and guide sprouting and reinnervation of neuromuscular junctions. Trends Neurosci. 19:280-285. doi:10.1016/S0166-2236(96)10032-1
94. Stent, G.S., and D.A. Weisblat. 1985. Cell lineage in the development of invertebrate nervous systems. Annu. Rev. Neurosci. 8:45-70. doi:10.1146/annurev. ne.08.030185.000401
95. Stout, C.E., J.L. Costantin, C.C. Naus, and A.C. Charles. 2002. Intercellular calcium signaling in astrocytes via ATP release through connexin hemichannels. J. Biol. Chem. 277:10482-10488. doi:10.1074/jbc.M109902200 (Pubitemid 34968170)
96. Suadicani, S.O., C.E. Flores, M. Urban-Maldonado, M. Beelitz, and E. Scemes. 2004. Gap junction channels coordinate the propagation of intercellular Ca2+ signals generated by P2Y receptor activation. Glia. 48:217-229. doi:10.1002/glia.20071 (Pubitemid 39545937)
97. Suadicani, S.O., C.F. Brosnan, and E. Scemes. 2006. P2X7 receptors mediate ATP release and amplification of astrocytic intercellular Ca2+ signaling. J. Neurosci. 26:1378-1385. doi:10.1523/JNEUROSCI.3902-05.2006 (Pubitemid 43237008)
98. Suadicani, S.O., R. Iglesias, D.C. Spray, and E. Scemes. 2009. Point mutation in the mouse P2X7 receptor affects intercellular calcium waves in astrocytes. ASN Neuro. 1.
99. Teves, M.E., H.A. Guidobaldi, D.R. Uñates, R. Sanchez, W. Miska, S.J. Publicover, A.A. Morales Garcia, and L.C. Giojalas. 2009. Molecular mechanism for human sperm chemotaxis mediated by progesterone. PLoS One. 4:e8211. doi:10.1371/journal.pone.0008211
100. Tornieri, K., and V. Rehder. 2007. Nitric oxide release from a single cell affects filopodial motility on growth cones of neighboring neurons. Dev. Neurobiol. 67:1932-1943. doi:10.1002/dneu.20572 (Pubitemid 350223928)
101. Veltman, D.M., and P.J. van Haastert. 2008. The role of cGMP and the rear of the cell in Dictyostelium chemotaxis and cell streaming. J. Cell Sci. 121:120-127. doi:10.1242/jcs.015602 (Pubitemid 351265709)
102. Verderio, C., and M. Matteoli. 2001. ATP mediates calcium signaling between astrocytes and microglial cells: modulation by IFNgamma. J. Immunol. 166:6383-6391.
103. Verkhratsky, A. 2006. Glial calcium signaling in physiology and pathophysiology. Acta Pharmacol. Sin. 27:773-780. doi:10.1111/j.1745-7254.2006. 00396.x (Pubitemid 44366009)
104. von Bernhardi, R., and K.J. Muller. 1995. Repair of the central nervous system: lessons from lesions in leeches. J. Neurobiol. 27:353-366. doi:10.1002/neu.480270308
105. Wang, X., G. Arcuino, T. Takano, J. Lin, W.G. Peng, P. Wan, P. Li, Q. Xu, Q.S. Liu, S.A. Goldman, and M. Nedergaard. 2004. P2X7 receptor inhibition improves recovery after spinal cord injury. Nat. Med. 10:821-827. doi:10.1038/nm1082 (Pubitemid 39070855)
106. Weisblat, D.A. 2007. Asymmetric cell divisions in the early embryo of the leech Helobdella robusta. Prog. Mol. Subcell. Biol. 45:79-95. doi:10.1007/978-3-540-69161-7-4
107. Yahyavi-Firouz-Abadi, N., P. Tahsili-Fahadan, and S.N. Ostad. 2007. Effect of mu and kappa opioids on injury-induced microglial accumulation in leech CNS: involvement of the nitric oxide pathway. Neuroscience. 144:1075-1086. doi:10.1016/j.neuroscience.2006.10.036
108. Yip, L., T. Woehrle, R. Corriden, M. Hirsh, Y. Chen, Y. Inoue, V. Ferrari, P.A. Insel, and W.G. Junger. 2009. Autocrine regulation of T-cell activation by ATP release and P2X7 receptors. FASEB J. 23:1685-1693. doi:10.1096/fj.08-126458