A critical role for pannexin-1 in activation of innate immune cells of the choroid plexus

Channels

Volumn 8, Issue 2, 2014, Pages 131-141

  Maslieieva, Valentyna ^a   Thompson, Roger J ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

ATP; Calcium; Chemotaxis; Choroid plexus; Epiplexus; Epithelial; Macrophage; P2X4; P2X7; Pannexin 1

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM ION; PANNEXIN 1; PROTEIN; PURINERGIC P2X4 RECEPTOR; PURINERGIC P2X7 RECEPTOR; UNCLASSIFIED DRUG; CALCIUM; GAP JUNCTION PROTEIN; NERVE PROTEIN; PANX1 PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; BLOOD CEREBROSPINAL FLUID BARRIER; CALCIUM TRANSPORT; CELL ACTIVATION; CELL ISOLATION; CELL MOTILITY; CELL MOTION; CHEMOKINESIS; CHOROID PLEXUS; CONTROLLED STUDY; EPIPLEXUS CELL; EPITHELIUM CELL; IMMUNOCOMPETENT CELL; INNATE IMMUNITY; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CHEMOTAXIS; CYTOLOGY; DRUG EFFECTS; GENETICS; HUMAN; IMMUNOLOGY; LUNG ALVEOLUS MACROPHAGE; METABOLISM; PHYSIOLOGY; SPRAGUE DAWLEY RAT; VIDEO MICROSCOPY;

ADENOSINE TRIPHOSPHATE; ANIMALS; CALCIUM; CELL MOVEMENT; CELLS, CULTURED; CHEMOTAXIS; CHOROID PLEXUS; CONNEXINS; HUMANS; MACROPHAGES, ALVEOLAR; MICROSCOPY, VIDEO; NERVE TISSUE PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, PURINERGIC P2X4; RECEPTORS, PURINERGIC P2X7;

EID: 84898876389     PISSN: 19336950     EISSN: 19336969     Source Type: Journal    
DOI: 10.4161/chan.27653     Document Type: Article

References (54)

1. Strazielle N, Ghersi-Egea JF. Choroid plexus in the central nervous system: biology and physiopathology. J Neuropathol Exp Neurol 2000; 59:561-74; PMID:10901227
2. Johanson CE, Stopa EG, McMillan PN. The blood-cerebrospinal fluid barrier: structure and functional significance. Methods Mol Biol 2011; 686:101-31; PMID:21082368; http://dx.doi.org/10.1007/978-1-60761-938-3-4
3. Ling EA, Kaur C, Lu J. Origin, nature, and some functional considerations of intraventricular macrophages, with special reference to the epiplexus cells. Microsc Res Tech 1998; 41:43-56; PMID:9550136; http://dx.doi.org/10.1002/(SICI) 1097-0029(19980401)41:1〈43::AID-JEMT5〉3.0.CO;2-V
4. Vercellino M, Votta B, Condello C, Piacentino C, Romagnolo A, Merola A, Capello E, Mancardi GL, Mutani R, Giordana MT, et al. Involvement of the choroid plexus in multiple sclerosis autoimmune inflammation: a neuropathological study. J Neuroimmunol 2008; 199:133-41; PMID:18539342; http://dx.doi.org/10. 1016/j.jneuroim.2008.04.035
5. Hosoya Y, Fujita T. Scanning electron microscope observation of intraventricular macrophages (Kolmer cells) in the rat brain. Arch Histol Jpn 1973; 35:133-40; PMID:4735623; http://dx.doi.org/10.1679/aohc1950.35.133
6. Ling EA. Ultrastruct and origin of epiplexus cells in the telencephalic choroid plexus of postnatal rats studied by intravenous injection of carbon particles. J Anat 1979; 129:479-92; PMID:541237
7. Guillemin GJ, Brew BJ. Microglia, macrophages, perivascular macrophages, and pericytes: a review of function and identification. J Leukoc Biol 2004; 75:388-97; PMID:14612429; http://dx.doi.org/10.1189/jlb.0303114
8. Schwarze EW. The origin of (Kolmer's) epiplexus cells. A combined histomorphological and histochemical study. Histochemistry 1975; 44:103-4; PMID:1181335; http://dx.doi.org/10.1007/BF00490425
9. McMenamin PG, Wealthall RJ, Deverall M, Cooper SJ, Griffin B. Macrophages and dendritic cells in the rat meninges and choroid plexus: three-dimensional localisation by environmental scanning electron microscopy and confocal microscopy. Cell Tissue Res 2003; 313:259-69; PMID:12920643; http://dx.doi.org/10.1007/s00441-003-0779-0
10. Melief J, Koning N, Schuurman KG, Van De Garde MDB, Smolders J, Hoek RM, Van Eijk M, Hamann J, Huitinga I. Phenotyping primary human microglia: tight regulation of LPS responsiveness. Glia 2012; 60:1506-17; PMID:22740309; http://dx.doi.org/10.1002/glia.22370
11. Lu J, Kaur C, Ling EA. Uptake of tracer by the epiplexus cells via the choroid plexus epithelium following an intravenous or intraperitoneal injection of horseradish peroxidase in rats. J Anat 1993; 183:609-17; PMID:8300438
12. Sivakumar V, Lu J, Ling EA, Kaur C. Vascular endothelial growth factor and nitric oxide production in response to hypoxia in the choroid plexus in neonatal brain. Brain Pathol 2008; 18:71-85; PMID:17924979; http://dx.doi.org/ 10.1111/j.1750-3639.2007.00104.x
13. Lu J, Kaur C, Ling EA. Up-regulation of surface antigens on epiplexus cells in postnatal rats following intraperitoneal injections of lipopolysaccharide. Neuroscience 1994; 63:1169-78; PMID:7700515; http://dx.doi.org/10.1016/0306-4522(94)90581-9
14. Lu J, Kaur C, Ling EA. Expression and upregulation of transferrin receptors and iron uptake in the epiplexus cells of different aged rats injected with lipopolysaccharide and interferon-gamma. J Anat 1995; 187:603-11; PMID:8586559
15. Lu J, Kaur C, Ling EA. Histochemical demonstration of nitric oxide synthase-like immunoreactivity in epiplexus cells and choroid epithelia in the lateral ventricles of postnatal rat brain induced by an intracerebral injection of lipopolysaccharide. Brain Res 1995; 699:275-85; PMID:8616631; http://dx.doi.org/10.1016/0006-8993(95)00919-H
16. Maxwell WL, Hardy IG, Watt C, McGadey J, Graham DI, Adams JH, Gennarelli TA. Changes in the choroid plexus, responses by intrinsic epiplexus cells and recruitment from monocytes after experimental head acceleration injury in the nonhuman primate. Acta Neuropathol 1992; 84:78-84; PMID:1502884; http://dx.doi.org/10.1007/BF00427218
17. Ling EA, Gopalakrishnakone P, Tan CK. Electron-microscopical study of the choroid plexus and epiplexus cells in cats following a cisternal injection of crotoxin complex. Acta Anat (Basel) 1988; 131:241-8; PMID:3376729; http://dx.doi.org/10.1159/000146523
18. Janeway CA Jr., Medzhitov R. Innate immune recognition. Annu Rev Immunol 2002; 20:197-216; PMID:11861602; http://dx.doi.org/10.1146/annurev.immunol.20. 083001.084359
19. Rubartelli A, Lotze MT. Inside, outside, upside down: damage-associated molecular-pattern molecules (DAMPs) and redox. Trends Immunol 2007; 28:429-36; PMID:17845865; http://dx.doi.org/10.1016/j.it.2007.08.004
20. Vitiello L, Gorini S, Rosano G, la Sala A. Immunoregulation through extracellular nucleotides. Blood 2012; 120:511-8; PMID:22661701; http://dx.doi.org/10.1182/blood-2012-01-406496
21. Franke H, Schepper C, Illes P, Krügel U. Involvement of P2X and P2Y receptors in microglial activation in vivo. Purinergic Signal 2007; 3:435-45; PMID:18404456; http://dx.doi.org/10.1007/s11302-007-9082-y
22. Kronlage M, Song J, Sorokin L, Isfort K, Schwerdtle T, Leipziger J, Robaye B, Conley PB, Kim H-C, Sargin S, et al. Autocrine purinergic receptor signaling is essential for macrophage chemotaxis. Sci Signal 2010; 3:ra55; PMID:20664064; http://dx.doi.org/10.1126/scisignal.2000588
23. Myrtek D, Müller T, Geyer V, Derr N, Ferrari D, Zissel G, Dürk T, Sorichter S, Luttmann W, Kuepper M, et al. Activation of human alveolar macrophages via P2 receptors: coupling to intracellular Ca2+ increases and cytokine secretion. J Immunol 2008; 181:2181-8; PMID:18641357
24. Sim JA, Park CK, Oh SB, Evans RJ, North RA. P2X1 and P2X4 receptor currents in mouse macrophages. Br J Pharmacol 2007; 152:1283-90; PMID:17934511; http://dx.doi.org/10.1038/sj.bjp.0707504
25. Elliott MR, Chekeni FB, Trampont PC, Lazarowski ER, Kadl A, Walk SF, Park D, Woodson RI, Ostankovich M, Sharma P, et al. Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature 2009; 461:282-6; PMID:19741708; http://dx.doi.org/10.1038/nature08296
26. Idzko M, Dichmann S, Ferrari D, Di Virgilio F, la Sala A, Girolomoni G, Panther E, Norgauer J. Nucleotides induce chemotaxis and actin polymerization in immature but not mature human dendritic cells via activation of pertussis toxin-sensitive P2y receptors. Blood 2002; 100:925-32; PMID:12130504; http://dx.doi.org/10.1182/blood.V100.3.925
27. Junger WG. Immune cell regulation by autocrine purinergic signalling. Nat Rev Immunol 2011; 11:201-12; PMID:21331080; http://dx.doi.org/10.1038/nri2938
28. Schenk U, Westendorf AM, Radaelli E, Casati A, Ferro M, Fumagalli M, Verderio C, Buer J, Scanziani E, Grassi F. Purinergic control of T cell activation by ATP released through pannexin-1 hemichannels. Sci Signal 2008; 1:ra6; PMID:18827222; http://dx.doi.org/10.1126/scisignal.1160583
29. Woehrle T, Yip L, Elkhal A, Sumi Y, Chen Y, Yao Y, Insel PA, Junger WG. Pannexin-1 hemichannel-mediated ATP release together with P2X1 and P2X4 receptors regulate T-cell activation at the immune synapse. Blood 2010; 116:3475-84; PMID:20660288; http://dx.doi.org/10.1182/blood-2010-04-277707
30. Pelegrin P, Surprenant A. Pannexin-1 mediates large pore formation and interleukin-1beta release by the ATP-gated P2X7 receptor. EMBO J 2006; 25:5071-82; PMID:17036048; http://dx.doi.org/10.1038/sj.emboj.7601378
31. Baroja-Mazo A, Barberà-Cremades M, Pelegrín P, Pelegrín P. The participation of plasma membrane hemichannels to purinergic signaling. Biochim Biophys Acta 2013; 1828:79-93; PMID:22266266; http://dx.doi.org/10.1016/j.bbamem.2012.01.002
32. Samuels SE, Lipitz JB, Dahl G, Muller KJ. Neuroglial ATP release through innexin channels controls microglial cell movement to a nerve injury. J Gen Physiol 2010; 136:425-42; PMID:20876360; http://dx.doi.org/10.1085/jgp.201010476
33. Samuels SE, Lipitz JB, Wang J, Dahl G, Muller KJ. Arachidonic acid closes innexin/pannexin channels and thereby inhibits microglia cell movement to a nerve injury. Dev Neurobiol 2013; 73:621-31; PMID:23650255; http://dx.doi.org/ 10.1002/dneu.22088
34. Sorokin SP, Hoyt RF Jr. Macrophage development: I. Rationale for using Griffonia simplicifolia isolectin B4 as a marker for the line. Anat Rec 1992; 232:520-6; PMID:1372795; http://dx.doi.org/10.1002/ar.1092320409
35. Dailey ME, Waite M. Confocal imaging of microglial cell dynamics in hippocampal slice cultures. Methods 1999; 18:222-30, 177; PMID:10356354; http://dx.doi.org/10.1006/meth.1999.0775
36. Streit WJ. An improved staining method for rat microglial cells using the lectin from Griffonia simplicifolia (GSA I-B4). J Histochem Cytochem 1990; 38:1683-6; PMID:2212623; http://dx.doi.org/10.1177/38.11.2212623
37. Ohsawa K, Imai Y, Kanazawa H, Sasaki Y, Kohsaka S. Involvement of Iba1 in membrane ruffling and phagocytosis of macrophages/microglia. J Cell Sci 2000; 113:3073-84; PMID:10934045
38. Imai Y, Ibata I, Ito D, Ohsawa K, Kohsaka S. A novel gene iba1 in the major histocompatibility complex class III region encoding an EF hand protein expressed in a monocytic lineage. Biochem Biophys Res Commun 1996; 224:855-62; PMID:8713135; http://dx.doi.org/10.1006/bbrc.1996.1112
39. Wilkinson PC. Assays of leukocyte locomotion and chemotaxis. J Immunol Methods 1998; 216:139-53; PMID:9760220; http://dx.doi.org/10.1016/S0022-1759(98) 00075-1
40. Hayoz S, Jia C, Hegg C. Mechanisms of constitutive and ATP-evoked ATP release in neonatal mouse olfactory epithelium. BMC Neurosci 2012; 13:53; PMID:22640172; http://dx.doi.org/10.1186/1471-2202-13-53
41. Locovei S, Bao L, Dahl G. Pannexin 1 in erythrocytes: function without a gap. Proc Natl Acad Sci U S A 2006; 103:7655-9; PMID:16682648; http://dx.doi.org/10.1073/pnas.0601037103
42. Chekeni FB, Elliott MR, Sandilos JK, Walk SF, Kinchen JM, Lazarowski ER, Armstrong AJ, Penuela S, Laird DW, Salvesen GS, et al. Pannexin 1 channels mediate 'find-me' signal release and membrane permeability during apoptosis. Nature 2010; 467:863-7; PMID:20944749; http://dx.doi.org/10.1038/nature09413
43. Wicki-Stordeur LE, Dzugalo AD, Swansburg RM, Suits JM, Swayne LA. Pannexin 1 regulates postnatal neural stem and progenitor cell proliferation. Neural Dev 2012; 7:11; PMID:22458943; http://dx.doi.org/10.1186/1749-8104-7-11
44. Penuela S, Bhalla R, Nag K, Laird DW. Glycosylation regulates pannexin intermixing and cellular localization. Mol Biol Cell 2009; 20:4313-23; PMID:19692571; http://dx.doi.org/10.1091/mbc.E09-01-0067
45. Weilinger NL, Tang PL, Thompson RJ. Anoxia-induced NMDA receptor activation opens pannexin channels via Src family kinases. J Neurosci 2012; 32:12579-88; PMID:22956847; http://dx.doi.org/10.1523/JNEUROSCI.1267-12.2012
46. Thompson RJ, Zhou N, MacVicar BA. Ischemia opens neuronal gap junction hemichannels. Science 2006; 312:924-7; PMID:16690868; http://dx.doi.org/10.1126/ science.1126241
47. Thompson RJ, Jackson MF, Olah ME, Rungta RL, Hines DJ, Beazely MA, MacDonald JF, MacVicar BA. Activation of pannexin-1 hemichannels augments aberrant bursting in the hippocampus. Science 2008; 322:1555-9; PMID:19056988; http://dx.doi.org/10.1126/science.1165209
48. Monif M, Burnstock G, Williams DA. Microglia: proliferation and activation driven by the P2X7 receptor. Int J Biochem Cell Biol 2010; 42:1753-6; PMID:20599520; http://dx.doi.org/10.1016/j.biocel.2010.06.021
49. Davalos D, Grutzendler J, Yang G, Kim JV, Zuo Y, Jung S, Littman DR, Dustin ML, Gan W-B. ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci 2005; 8:752-8; PMID:15895084; http://dx.doi.org/10.1038/ nn1472
50. Xiang Z, Burnstock G. Expression of P2X receptors in rat choroid plexus. Neuroreport 2005; 16:903-7; PMID:15931059; http://dx.doi.org/10.1097/00001756- 200506210-00006
51. Qiu F, Dahl G. A permeant regulating its permeation pore: inhibition of pannexin 1 channels by ATP. Am J Physiol Cell Physiol 2009; 296:C250-5; PMID:18945939; http://dx.doi.org/10.1152/ajpcell.00433.2008
52. Wiley JS, Sluyter R, Gu BJ, Stokes L, Fuller SJ. The human P2X7 receptor and its role in innate immunity. Tissue Antigens 2011; 78:321-32; PMID:21988719; http://dx.doi.org/10.1111/j.1399-0039.2011.01780.x
53. Di Virgilio F. Liaisons dangereuses: P2X(7) and the inflammasome. Trends Pharmacol Sci 2007; 28:465-72; PMID:17692395; http://dx.doi.org/10.1016/j.tips. 2007.07.002
54. Locovei S, Wang J, Dahl G. Activation of pannexin 1 channels by ATP through P2Y receptors and by cytoplasmic calcium. FEBS Lett 2006; 580:239-44; PMID:16364313; http://dx.doi.org/10.1016/j.febslet.2005.12.004