ATP is required and advances cytokine-induced gap junction formation in microglia in vitro

Mediators of Inflammation

Volumn 2013, Issue , 2013, Pages

  Sáez, Pablo J ^a,b   Shoji, Kenji F ^a,b   Retamal, Mauricio A ^c   Harcha, Paloma A ^a,b   Ramírez, Gigliola ^d   Jiang, Jean X ^e   Von Bernhardi, Rommy ^d   Sáez, Juan C ^a,b  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b Centro Interdisciplinario de Neurociencias de Valparaíso   (Chile)

^c UNIVERSIDAD DEL DESARROLLO   (Chile)

^d PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^e UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CONNEXIN 43; CYTOKINE; DYE; GAMMA INTERFERON; GAP JUNCTION PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; PANNEXIN 1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; AUTOCRINE EFFECT; CELL COMMUNICATION; CELL FUNCTION; CELL LINE; CONTROLLED STUDY; CROSS COUPLING REACTION; CYTOKINE RELEASE; EXTRACELLULAR MATRIX; GAP JUNCTION; GAP JUNCTION CHANNEL; HEMICHANNEL; IMMUNE RESPONSE; IN VITRO STUDY; MICROGLIA; MOLECULAR DOCKING; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INDUCTION; ANIMAL; CELL CULTURE; CYTOLOGY; DRUG EFFECT; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENT ANTIBODY TECHNIQUE; METABOLISM; MOUSE; RAT; WESTERN BLOTTING; DRUG EFFECTS;

ADENOSINE TRIPHOSPHATE; ANIMALS; BLOTTING, WESTERN; CELL LINE; CELLS, CULTURED; CYTOKINES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLUORESCENT ANTIBODY TECHNIQUE; GAP JUNCTIONS; INTERFERON-GAMMA; INTERLEUKIN-1BETA; INTERLEUKIN-6; MICE; MICROGLIA; RATS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84877970834     PISSN: 09629351     EISSN: 14661861     Source Type: Journal    
DOI: 10.1155/2013/216402     Document Type: Article

References (80)

1. Kettenmann H., Hanisch U. K., Noda M., Verkhratsky A., Physiology of microglia. Physiological Reviews 2011 91 461 553
2. Ransohoff R. M., Perry V. H., Microglial physiology: unique stimuli, specialized responses. Annual Review of Immunology 2009 27 119 145 2-s2.0-67650966680 10.1146/annurev.immunol.021908.132528
3. Inoue K., Purinergic systems in microglia. Cellular and Molecular Life Sciences 2008 65 19 3074 3080 2-s2.0-53049107855 10.1007/s00018-008-8210-3
4. Von Bernhardi R., Tichauer J. E., Eugenín J., Aging-dependent changes of microglial cells and their relevance for neurodegenerative disorders. Journal of Neurochemistry 2010 112 5 1099 1114 2-s2.0-75949127404 10.1111/j.1471-4159.2009.06537.x
5. Barger S. W., Basile A. S., Activation of microglia by secreted amyloid precursor protein evokes release of glutamate by cystine exchange and attenuates synaptic function. Journal of Neurochemistry 2001 76 3 846 854 2-s2.0-0035146889 10.1046/j.1471-4159.2001.00075.x (Pubitemid 32126084)
6. De Simone R., Levi G., Aloisi F., Interferon γ gene expression in rat central nervous system glial cells. Cytokine 1998 10 6 418 422 2-s2.0-0032101935 10.1006/cyto.1997.0314 (Pubitemid 28276787)
7. Hanisch U. K., Microglia as a source and target of cytokines. Glia 2002 40 2 140 155 2-s2.0-0036849018 10.1002/glia.10161 (Pubitemid 35337372)
8. Soo Y. K., Ju H. M., Hwan G. L., Seung U. K., Yong B. L., ATP released from β -amyloid-stimulated microglia induces reactive oxygen species production in an autocrine fashion. Experimental and Molecular Medicine 2007 39 6 820 827 2-s2.0-38049188027
9. Piani D., Fontana A., Involvement of the cystine transport system xc/- in the macrophage-induced glutamate-dependent cytotoxicity to neurons. Journal of Immunology 1994 152 7 3578 3585 2-s2.0-0028297676
10. Chao C. C., Hu S., Ehrlich L., Peterson P. K., Interleukin-1 and tumor necrosis factor- α synergistically mediate neurotoxicity: involvement of nitric oxide and of N-methyl-D-aspartate receptors. Brain, Behavior, and Immunity 1995 9 4 355 365 2-s2.0-0029620390 10.1006/brbi.1995.1033 (Pubitemid 26039774)
11. Gendron F. P., Chalimoniuk M., Strosznajder J., Shen S., González F. A., Weisman G. A., Sun G. Y., P2X7 nucleotide receptor activation enhances IFN γ -induced type II nitric oxide synthase activity in BV-2 microglial cells. Journal of Neurochemistry 2003 87 2 344 352 2-s2.0-0141884377 10.1046/j.1471-4159.2003.01995.x (Pubitemid 37255242)
12. Kuno R., Wang J., Kawanokuchi J., Takeuchi H., Mizuno T., Suzumura A., Autocrine activation of microglia by tumor necrosis factor- α Journal of Neuroimmunology 2005 162 1-2 89 96 2-s2.0-17044396389 10.1016/j.jneuroim.2005. 01.015
13. Inoue K., Microglial activation by purines and pyrimidines. Glia 2002 40 2 156 163 2-s2.0-0036848882 10.1002/glia.10150 (Pubitemid 35337373)
14. Bianco F., Pravettoni E., Colombo A., Schenk U., Möller T., Matteoli M., Verderio C., Astrocyte-derived ATP induces vesicle shedding and IL-1 β release from microglia. Journal of Immunology 2005 174 11 7268 7277 2-s2.0-18944380607 (Pubitemid 40705696)
15. 2+ waves trigger responses in microglial cells in brain slices. The FASEB Journal 2002 16 2 255 257 2-s2.0-0036484251
16. Verderio C., Matteoli M., ATP mediates calcium signaling between astrocytes and microglial cells: modulation by IFN- γ Journal of Immunology 2001 166 10 6383 6391 2-s2.0-0035873729 (Pubitemid 32440772)
17. 7 receptor expression. Journal of Immunology 2009 182 7 4378 4385 2-s2.0-64249169414 10.4049/jimmunol.0803612
18. 7 purinergic receptor: from physiology to neurological disorders. FASEB Journal 2010 24 2 337 345 2-s2.0-76149099290 10.1096/fj.09-138883
19. Ferrari D., Chiozzi P., Falzoni S., Hanau S., Di Virgilio F., Purinergic modulation of interleukin-1 β release from microglial cells stimulated with bacterial endotoxin. Journal of Experimental Medicine 1997 185 3 579 582 2-s2.0-0031054641 10.1084/jem.185.3.579 (Pubitemid 27078376)
20. Seo D. R., Kim K. Y., Lee Y. B., Interleukin-10 expression in lipopolysaccharide-activated microglia is mediated by extracellular ATP in an autocrine fashion. NeuroReport 2004 15 7 1157 1161 2-s2.0-2442718746 10.1097/00001756-200405190-00015 (Pubitemid 38670072)
21. Färber K., Kettenmann H., Functional role of calcium signals for microglial function. Glia 2006 54 7 656 665 2-s2.0-33750305578 10.1002/glia.20412 (Pubitemid 44629629)
22. Hoffmann A., Kann O., Ohlemeyer C., Hanisch U. K., Kettenmann H., Elevation of basal intracellular calcium as a central element in the activation of brain macrophages (microglia): suppression of receptor-evoked calcium signaling and control of release function. Journal of Neuroscience 2003 23 11 4410 4419 2-s2.0-0038795206 (Pubitemid 36706171)
23. Eugenín E. A., Eckardt D., Theis M., Willecke K., Bennett M. V. L., Sáez J. C., Microglia at brain stab wounds express connexin 43 and in vitro form functional gap junctions after treatment with interferon- γ and tumor necrosis factor- α Proceedings of the National Academy of Sciences of the United States of America 2001 98 7 4190 4195 2-s2.0-0035957352 10.1073/pnas.051634298 (Pubitemid 32249920)
24. Martínez A. D., Eugenín E. A., Brañes M. C., Bennett M. V., Sáez J. C., Identification of second messengers that induce expression of functional gap junctions in microglia cultured from newborn rats. Brain Research 2002 943 191 201 (Pubitemid 36120379)
25. Orellana J. A., Sáez P. J., Shoji K. F., Schalper K. A., Palacios-Prado N., Velarde V., Giaume C., Bennett M. V. L., Sáez J. C., Modulation of brain hemichannels and gap junction channels by pro-inflammatory agents and their possible role in neurodegeneration. Antioxidants and Redox Signaling 2009 11 2 369 399 2-s2.0-58149100746 10.1089/ars.2008.2130
26. Dobrenis K., Chang H. Y., Pina-Benabou M. H., Woodroffe A., Lee S. C., Rozental R., Spray D. C., Scemes E., Human and mouse microglia express connexin36, and functional gap junctions are formed between rodent microglia and neurons. Journal of Neuroscience Research 2005 82 3 306 315 2-s2.0-27644524673 10.1002/jnr.20650 (Pubitemid 41552482)
27. Garg S., Syed M. M., Kielian T., Staphylococcus aureus-derived peptidoglycan induces Cx43 expression and functional gap junction intercellular communication in microglia. Journal of Neurochemistry 2005 95 2 475 483 2-s2.0-26844515789 10.1111/j.1471-4159.2005.03384.x (Pubitemid 41457516)
28. Shaikh S. B., Uy B., Perera A., Nicholson L. F., AGEs-RAGE mediated up-regulation of connexin43 in activated human microglial CHME-5 cells. Neurochemistry International 2012 60 6 640 651
29. Panchin Y. V., Evolution of gap junction proteins-the pannexin alternative. Journal of Experimental Biology 2005 208 8 1415 1419 2-s2.0-18944394972 10.1242/jeb.01547 (Pubitemid 40697529)
30. Locovei S., Wang J., Dahl G., Activation of pannexin 1 channels by ATP through P2Y receptors and by cytoplasmic calcium. FEBS Letters 2006 580 1 239 244 2-s2.0-29344452180 10.1016/j.febslet.2005.12.004 (Pubitemid 43005343)
31. 7 receptor. EMBO Journal 2006 25 21 5071 5082 2-s2.0-33750473352 10.1038/sj.emboj.7601378 (Pubitemid 44658525)
32. Bao L., Locovei S., Dahl G., Pannexin membrane channels are mechanosensitive conduits for ATP. FEBS Letters 2004 572 1-3 65 68 2-s2.0-4143127920 10.1016/j.febslet.2004.07.009 (Pubitemid 39092514)
33. Davalos D., Grutzendler J., Yang G., Kim J. V., Zuo Y., Jung S., Littman D. R., Dustin M. L., Gan W. B., ATP mediates rapid microglial response to local brain injury in vivo. Nature Neuroscience 2005 8 6 752 758 2-s2.0-22244464662 10.1038/nn1472 (Pubitemid 43085841)
34. Fontainhas A. M., Wang M., Liang K. J., Chen S., Mettu P., Damani M., Fariss R. N., Li W., Wong W. T., Microglial morphology and dynamic behavior is regulated by ionotropic glutamatergic and GABAergic neurotransmission. PLoS ONE 2011 6 1, article e15973 2-s2.0-79551570269 10.1371/journal.pone.0015973
35. Orellana J. A., Shoji K. F., Abudara V., Ezan P., Amigou E., Sáez P. J., Jiang J. X., Naus C. C., Sáez J. C., Giaume C., Amyloid β -induced death in neurons involves glial and neuronal hemichannels. Journal of Neuroscience 2011 31 13 4962 4977 2-s2.0-79955739803 10.1523/JNEUROSCI.6417-10. 2011
36. Froger N., Orellana J. A., Calvo C. F., Amigou E., Kozoriz M. G., Naus C. C., Sáez J. C., Giaume C., Inhibition of cytokine-induced connexin43 hemichannel activity in astrocytes is neuroprotective. Molecular and Cellular Neuroscience 2010 45 1 37 46 2-s2.0-77955091332 10.1016/j.mcn.2010.05.007
37. Orellana J. A., Froger N., Ezan P., ATP and glutamate released via astroglial connexin 43 hemichannels mediate neuronal death through activation of pannexin 1 hemichannels. Journal of Neurochemistry 2011 118 826 840
38. Retamal M. A., Froger N., Palacios-Prado N., Ezan P., Sáez P. J., Sáez J. C., Giaume C., Cx43 hemichannels and gap junction channels in astrocytes are regulated oppositely by proinflammatory cytokines released from activated microglia. Journal of Neuroscience 2007 27 50 13781 13792 2-s2.0-37249015389 10.1523/JNEUROSCI.2042-07.2007 (Pubitemid 350278255)
39. Buvinic S., Almarza G., Bustamante M., Casas M., López J., Riquelme M., Sáez J. C., Huidobro-Toro J. P., Jaimovich E., ATP released by electrical stimuli elicits calcium transients and gene expression in skeletal muscle. Journal of Biological Chemistry 2009 284 50 34490 34505 2-s2.0-71749095578 10.1074/jbc.M109.057315
40. Cea L. A., Riquelme M. A., Cisterna B. A., Connexin- and pannexin-based channels in normal skeletal muscles and their possible role in muscle atrophy. Journal of Membrane Biology 2012 245 423 436
41. Brañes M. C., Contreras J. E., Sáez J. C., Activation of human polymorphonuclear cells induces formation of functional gap junctions and expression of connexins. Medical Science Monitor 2002 8 BR313 BR323 (Pubitemid 34951421)
42. Bao B., Jiang J., Yanase T., Nishi Y., Morgan J. R., Connexon-mediated cell adhesion drives microtissue self-assembly. FASEB Journal 2011 25 1 255 264 2-s2.0-79251572022 10.1096/fj.10-155291
43. + T cells. Journal of Neuroimmunology 1995 63 2 163 174 2-s2.0-0029563373 10.1016/0165-5728(95)00146-8 (Pubitemid 26019010)
44. Sklar M. D., Tereba A., Chen B. D. M., Walker W. S., Transformation of mouse bone marrow cells by transfection with a human oncogene related to c-myc is associated with the endogenous production of macrophage colony stimulating factor 1. Journal of Cellular Physiology 1985 125 3 403 412 2-s2.0-0022340655 (Pubitemid 16200935)
45. i responses. Molecular Biology of the Cell 2008 19 8 3501 3513 2-s2.0-54249087709 10.1091/mbc.E07-12-1240
46. 2+ exchange activity by interferon- γ in cultured rat microglia. Journal of Neurochemistry 2004 90 4 784 791 2-s2.0-4143139724 10.1111/j.1471-4159.2004.02511.x (Pubitemid 39099959)
47. Franciosi S., Choi H. B., Kim S. U., McLarnon J. G., Interferon- γ acutely induces calcium influx in human microglia. Journal of Neuroscience Research 2002 69 5 607 613 2-s2.0-0036708172 10.1002/jnr.10331 (Pubitemid 34966873)
48. Möller T., Calcium signaling in microglial cells. Glia 2002 40 2 184 194 2-s2.0-0036847845 10.1002/glia.10152 (Pubitemid 35337376)
49. + currents in human microglia. Neuroscience 2001 104 4 1175 1184 2-s2.0-0035800001 10.1016/S0306-4522(01)00119-1 (Pubitemid 32701976)
50. Corvalán L. A., Araya R., Brañes M. C., Injury of skeletal muscle and specific cytokines induce the expression of gap junction channels in mouse dendritic cells. Journal of Cellular Physiology 2007 211 649 660 (Pubitemid 46683033)
51. Eugenín E. A., Brañes M. C., Berman J. W., Sáez J. C., TNF- α plus IFN- γ induce connexin43 expression and formation of gap junctions between human monocytes/macrophages that enhance physiological responses. Journal of Immunology 2003 170 3 1320 1328 2-s2.0-0037307922 (Pubitemid 36139499)
52. Shigemoto-Mogami Y., Koizumi S., Tsuda M., Ohsawa K., Kohsaka S., Inoue K., Mechanisms underlying extracellular ATP-evoked interleukin-6 release in mouse microglial cell line, MG-5. Journal of Neurochemistry 2001 78 6 1339 1349 2-s2.0-0034814542 10.1046/j.1471-4159.2001.00514.x (Pubitemid 32899765)
53. North R. A., Molecular physiology of P2X receptors. Physiological Reviews 2002 82 4 1013 1067 2-s2.0-0036788971
54. 2+ mobilization and functional responses in microglia: effects of low levels of ATP. Journal of Neuroscience Research 2005 81 3 349 356 2-s2.0-25444444697 10.1002/jnr.20475 (Pubitemid 41359289)
55. Pousset F., Palin K., Verrier D., Bristow A., Dantzer R., Parnet P., Lestage J., Production of interleukin-1 receptor antagonist isoforms by microglia in mixed rat glial cells stimulated by lipopolysaccharide. European Cytokine Network 2000 11 4 682 689 2-s2.0-0034523053 (Pubitemid 32044255)
56. Takeuchi H., Jin S., Wang J., Zhang G., Kawanokuchi J., Kuno R., Sonobe Y., Mizuno T., Suzumura A., Tumor necrosis factor- α induces neurotoxicity via glutamate release from hemichannels of activated microglia in an autocrine manner. Journal of Biological Chemistry 2006 281 30 21362 21368 2-s2.0-33746354022 10.1074/jbc.M600504200 (Pubitemid 44115475)
57. Takeuchi H., Mizoguchi H., Doi Y., Jin S., Noda M., Liang J., Li H., Zhou Y., Mori R., Yasuoka S., Li E., Parajuli B., Kawanokuchi J., Sonobe Y., Sato J., Yamanaka K., Sobue G., Mizuno T., Suzumura A., Blockade of gap junction hemichannel suppresses disease progression in mouse models of amyotrophic lateral sclerosis and Alzheimer's disease. PLoS ONE 2011 6 6, article e21108 2-s2.0-79959359691 10.1371/journal.pone.0021108
58. Yawata I., Takeuchi H., Doi Y., Liang J., Mizuno T., Suzumura A., Macrophage-induced neurotoxicity is mediated by glutamate and attenuated by glutaminase inhibitors and gap junction inhibitors. Life Sciences 2008 82 21-22 1111 1116 2-s2.0-43049125769 10.1016/j.lfs.2008.03.010
59. Contreras J. E., Sánchez H. A., Eugenin E. A., Speidel D., Theis M., Willecke K., Bukauskas F. F., Bennett M. V. L., Sáez J. C., Metabolic inhibition induces opening of unapposed connexin 43 gap junction hemichannels and reduces gap junctional communication in cortical astrocytes in culture. Proceedings of the National Academy of Sciences of the United States of America 2002 99 1 495 500 2-s2.0-0037039391 10.1073/pnas.012589799 (Pubitemid 34060389)
60. Bruzzone R., Barbe M. T., Jakob N. J., Monyer H., Pharmacological properties of homomeric and heteromeric pannexin hemichannels expressed in Xenopus oocytes. Journal of Neurochemistry 2005 92 5 1033 1043 2-s2.0-14844334146 10.1111/j.1471-4159.2004.02947.x (Pubitemid 40344294)
61. Ferrari D., Villalba M., Chiozzi P., Falzoni S., Ricciardi-Castagnoli P., Di Virgilio F., Mouse microglial cells express a plasma membrane pore gated by extracellular ATP. Journal of Immunology 1996 156 4 1531 1539 2-s2.0-0030022576 (Pubitemid 26065865)
62. 7 receptor drives microglial activation and proliferation: a trophic role for P2X7R pore. Journal of Neuroscience 2009 29 12 3781 3791 2-s2.0-64849087753 10.1523/JNEUROSCI.5512-08.2009
63. 7 receptor activacion induces reactive oxygen species formation and cell death in murine EOC13 microglia. Mediators of Inflammation 2013 2013 18 271813
64. Kang J., Kang N., Lovatt D., Torres A., Zhao Z., Lin J., Nedergaard M., Connexin 43 hemichannels are permeable to ATP. Journal of Neuroscience 2008 28 18 4702 4711 2-s2.0-44649092806 10.1523/JNEUROSCI.5048-07.2008
65. Beahm D. L., Hall J. E., Opening hemichannels in nonjunctional membrane stimulates gap junction formation. Biophysical Journal 2004 86 2 781 796 2-s2.0-1142274309 (Pubitemid 38209524)
66. Siller-Jackson A. J., Burra S., Gu S., Xia X., Bonewald L. F., Sprague E., Jiang J. X., Adaptation of connexin 43-hemichannel prostaglandin release to mechanical loading. Journal of Biological Chemistry 2008 283 39 26374 26382 2-s2.0-55549123031 10.1074/jbc.M803136200
67. Decrock E., Vinken M., Bol M., Calcium and connexin-based intercellular communication, a deadly catch? Cell Calcium 2011 50 310 321
68. 2+ regulation of connexin 43 hemichannels in C6 glioma and glial cells. Cell Calcium 2009 46 3 176 187 2-s2.0-69249213411 10.1016/j.ceca.2009.07.002
69. 2+ permeability in Cx26 hemichannels formed by the A40V and G45E mutations that cause keratitis ichthyosis deafness syndrome. Journal of General Physiology 2010 136 1 47 62 2-s2.0-77954320871 10.1085/jgp.201010433
70. 2+ influx induced by extracellular alkalinization. American Journal of Physiology 2010 299 6 C1504 C1515 2-s2.0-78649653091 10.1152/ajpcell.00015. 2010
71. Vanden Abeele F., Bidaux G., Gordienko D., Beck B., Panchin Y. V., Baranova A. V., Ivanov D. V., Skryma R., Prevarskaya N., Functional implications of calcium permeability of the channel formed by pannexin 1. Journal of Cell Biology 2006 174 4 535 546 2-s2.0-33747160473 10.1083/jcb.200601115 (Pubitemid 44231865)
72. Mendoza-Naranjo A., Saéz P. J., Johansson C. C., Ramírez M., Mandaković D., Pereda C., López M. N., Kiessling R., Sáez J. C., Salazar-Onfray F., Functional gap junctions facilitate melanoma antigen transfer and cross-presentation between human dendritic cells. Journal of Immunology 2007 178 11 6949 6957 2-s2.0-34249811507 (Pubitemid 46847421)
73. Ásgeirsson K. S., Ólafsdóttir K., Jónasson J. G., Ógmundsdóttir H. M., The effects of IL-6 on cell adhesion and E-cadherin expression in breast cancer. Cytokine 1998 10 9 720 728 2-s2.0-0032169130 10.1006/cyto.1998.0349 (Pubitemid 28457117)
74. Tsuda M., Masuda T., Kitano J., Shimoyama H., Tozaki-Saitoh H., Inoue K., IFN- γ receptor signaling mediates spinal microglia activation driving neuropathic pain. Proceedings of the National Academy of Sciences of the United States of America 2009 106 19 8032 8037 2-s2.0-66049164016 10.1073/pnas. 0810420106
75. Takenouchi T., Sugama S., Iwamaru Y., Hashimoto M., Kitani H., Modulation of the ATP-lnduced release and processing of IL-1 Β in microglial cells. Critical Reviews in Immunology 2009 29 4 335 345 2-s2.0-69149106095
76. Garré J. M., Retamal M. A., Cassina P., Barbeito L., Bukauskas F. F., Sáez J. C., Bennett M. V. L., Abudara V., FGF-1 induces ATP release from spinal astrocytes in culture and opens pannexin and connexin hemichannels. Proceedings of the National Academy of Sciences of the United States of America 2010 107 52 22659 22664 2-s2.0-78651081496 10.1073/pnas.1013793107
77. Iwabuchi S., Kawahara K., Functional significance of the negative-feedback regulation of ATP release via pannexin-1 hemichannels under ischemic stress in astrocytes. Neurochemistry International 2011 58 3 376 384 2-s2.0-79951580400 10.1016/j.neuint.2010.12.013
78. 2+ waves transmit brain-damage signals to microglia. Developmental Cell 2012 22 1138 1148
79. Rigato C., Swinnen N., Buckinx R., Microglia proliferation is controlled by P2X7 receptors in a Pannexin-1-independent manner during early embryonic spinal cord invasion. The Journal of Neuroscience 2012 32 11559 11573
80. Quintanilla R. A., Orellana J. A., von Bernhardi R., Understanding risk factors for Alzheimer's disease: interplay of neuroinflammation, connexin-based communication and oxidative stress. Archives of Medical Research 2012 43 632 644