Genetically dissecting P2rx7 expression within the central nervous system using conditional humanized mice

Purinergic Signalling

Volumn 13, Issue 2, 2017, Pages 153-170

  Metzger, Michael W ^a   Walser, Sandra M ^a   Aprile Garcia, Fernando ^b,c   Dedic, Nina ^a   Chen, Alon ^a,d   Holsboer, Florian ^a,e   Arzt, Eduardo ^b   Wurst, Wolfgang ^f,g,h,i   Deussing, Jan M ^a  

^a MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

^b Instituto de Investigación en Biomedicina de Buenos Aires   (Argentina)

^c MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

^d INSTITUTE OF EPIDEMIOLOGY   (Germany)

^e HMNC GmbH   (Germany)

^f GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^g UNIVERSITY OF MUNICH   (Germany)

^h WEIZMANN INSTITUTE OF SCIENCE   (Israel)

ⁱ TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Gene expression; Knockout; Mouse model; P2rx7 gene; P2X7 receptor; Pore formation

Indexed keywords

COMPLEMENTARY DNA; INTERLEUKIN 1BETA; NEUROLEPTIC AGENT; PURINERGIC P2X7 RECEPTOR; P2RX7 PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; BRAIN; CALCIUM TRANSPORT; CELLULAR DISTRIBUTION; CENTRAL NERVOUS SYSTEM; CONFOCAL MICROSCOPY; GENE; GENE EXPRESSION; GENE SEQUENCE; GENOTYPE; IN SITU HYBRIDIZATION; MOUSE; NONHUMAN; P2RX7 GENE; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOUTHERN BLOTTING; WESTERN BLOTTING; ANIMAL; ANIMAL MODEL; GENE KNOCK-IN; HUMAN; KNOCKOUT MOUSE; METABOLISM;

ANIMALS; BRAIN; GENE KNOCK-IN TECHNIQUES; HUMANS; MICE; MICE, KNOCKOUT; MODELS, ANIMAL; RECEPTORS, PURINERGIC P2X7;

EID: 84995743463     PISSN: 15739538     EISSN: 15739546     Source Type: Journal    
DOI: 10.1007/s11302-016-9546-z     Document Type: Article

References (68)

1. Khakh BS, North RA (2006) P2X receptors as cell-surface ATP sensors in health and disease. Nature 442:527–532. doi:10.1038/nature04886
2. Kaczmarek-Hájek K, Lörinczi E, Hausmann R, Nicke A (2012) Molecular and functional properties of P2X receptors--recent progress and persisting challenges. Purinergic Signal 8:375–417. doi:10.1007/s11302-012-9314-7
3. Surprenant A, Rassendren F, Kawashima E et al (1996) The cytolytic P2Z receptor for extracellular ATP identified as a P2X receptor (P2X7). Science 272:735–738. doi:10.1126/science.272.5262.735
4. Chessell IP, Simon J, Hibell AD et al (1998) Cloning and functional characterisation of the mouse P2X7 receptor. FEBS Lett 439:26–30. doi:10.1016/S0014-5793(98)01332-5
5. Bradley HJ, Baldwin JM, Goli GR et al (2011) Residues 155 and 348 contribute to the determination of P2X7 receptor function via distinct mechanisms revealed by single-nucleotide polymorphisms. J Biol Chem 286:8176–8187. doi:10.1074/jbc.M110.211284
6. Denlinger LC, Fisette PL, Sommer JA et al (2001) Cutting edge: the nucleotide receptor P2X7 contains multiple protein- and lipid-interaction motifs including a potential binding site for bacterial lipopolysaccharide. J Immunol 167:1871–1876. doi:10.4049/jimmunol.167.4.1871
7. Nicke A, Kuan YH, Masin M et al (2009) A functional P2X7 splice variant with an alternative transmembrane domain 1 escapes gene inactivation in P2X7 knock-out mice. J Biol Chem 284:25813–25822. doi:10.1074/jbc.M109.033134
8. Hibell AD, Thompson KM, Simon J et al (2001) Species- and agonist-dependent differences in the deactivation-kinetics of P2X7 receptors. Naunyn Schmiedeberg's Arch Pharmacol 363:639–648. doi:10.1007/s002100100412
9. Donnelly-Roberts DL, Namovic MT, Han P, Jarvis MF (2009) Mammalian P2X7 receptor pharmacology: comparison of recombinant mouse, rat and human P2X7 receptors. Br J Pharmacol 157:1203–1214. doi:10.1111/j.1476-5381.2009.00233.x
10. Nörenberg W, Sobottka H, Hempel C et al (2012) Positive allosteric modulation by ivermectin of human but not murine P2X7 receptors. Br J Pharmacol 167:48–66. doi:10.1111/j.1476-5381.2012.01987.x
11. Hempel C, Nörenberg W, Sobottka H et al (2013) The phenothiazine-class antipsychotic drugs prochlorperazine and trifluoperazine are potent allosteric modulators of the human P2X7 receptor. Neuropharmacology 75:365–379. doi:10.1016/j.neuropharm.2013.07.027
12. Masin M, Young C, Lim K et al (2012) Expression, assembly and function of novel C-terminal truncated variants of the mouse P2X7 receptor: re-evaluation of P2X7 knockouts. Br J Pharmacol 165:978–993. doi:10.1111/j.1476-5381.2011.01624.x
13. Schwarz N, Drouot L, Nicke A et al (2012) Alternative splicing of the N-terminal cytosolic and transmembrane domains of P2X7 controls gating of the Ion Channel by ADP-ribosylation. PLoS One 7:e41269. doi:10.1371/journal.pone.0041269
14. Kido Y, Kawahara C, Terai Y et al (2013) Regulation of activity of P2X7 receptor by its splice variants in cultured mouse astrocytes. Glia:1–12. doi:10.1002/glia.22615
15. North RA (2002) Molecular physiology of P2X receptors. Physiol Rev 82:1013–1067. doi:10.1152/physrev.00015.2002
16. Adinolfi E, Callegari MG, Ferrari D et al (2005) Basal activation of the P2X7 ATP receptor elevates mitochondrial calcium and potential, increases cellular ATP levels, and promotes serum-independent growth. Mol Biol Cell 16:3260–3272. doi:10.1091/mbc.E04-11-1025
17. Xu XJ, Boumechache M, Robinson LE et al (2012) Splice variants of the P2X7 receptor reveal differential agonist dependence and functional coupling with pannexin-1. J Cell Sci 125:3776–3789. doi:10.1242/jcs.099374
18. Burnstock G, Knight GE (2004) Cellular distribution and functions of P2 receptor subtypes in different systems. Int Rev Cytol 240:31–304. doi:10.1016/S0074-7696(04)40002-3
19. Wiley JS, Sluyter R, Gu BJ et al (2011) The human P2X7 receptor and its role in innate immunity. Tissue Antigens 78:321–332. doi:10.1111/j.1399-0039.2011.01780.x
20. Anderson CM, Nedergaard M (2006) Emerging challenges of assigning P2X7 receptor function and immunoreactivity in neurons. Trends Neurosci 29:257–262. doi:10.1016/j.tins.2006.03.003
21. Deuchars SA, Atkinson L, Brooke RE et al (2001) Neuronal P2X7 receptors are targeted to presynaptic terminals in the central and peripheral nervous systems. J Neurosci 21:7143–7152
22. Miras-Portugal MT, Diaz-Hernandez M, Giraldez L et al (2003) P2X7 receptors in rat brain: presence in synaptic terminals and granule cells. Neurochem Res 28:1597–1605. doi:10.1023/A:1025690913206
23. Solle M, Labasi J, Perregaux DG et al (2001) Altered cytokine production in mice lacking P2X(7) receptors. J Biol Chem 276:125–132. doi:10.1074/jbc.M006781200
24. Chessell IP, Hatcher JP, Bountra C et al (2005) Disruption of the P2X7 purinoceptor gene abolishes chronic inflammatory and neuropathic pain. Pain 114:386–396. doi:10.1016/j.pain.2005.01.002
25. Sim JA, Young MT, Sung H-Y et al (2004) Reanalysis of P2X7 receptor expression in rodent brain. J Neurosci 24:6307–6314. doi:10.1523/JNEUROSCI.1469-04.2004
26. Sánchez-Nogueiro J, Marín-García P, Miras-Portugal MT (2005) Characterization of a functional P2X(7)-like receptor in cerebellar granule neurons from P2X(7) knockout mice. FEBS Lett 579:3783–3788. doi:10.1016/j.febslet.2005.05.073
27. Taylor SRJ, Gonzalez-Begne M, Sojka DK et al (2009) Lymphocytes from P2X7-deficient mice exhibit enhanced P2X7 responses. J Leukoc Biol 85:978–986. doi:10.1189/jlb.0408251
28. Marín-García P, Sánchez-Nogueiro J, Gómez-Villafuertes R et al (2008) Synaptic terminals from mice midbrain exhibit functional P2X7 receptor. Neuroscience 151:361–373. doi:10.1016/j.neuroscience.2007.10.038
29. Basso AM, Bratcher NA, Harris RR et al (2009) Behavioral profile of P2X7 receptor knockout mice in animal models of depression and anxiety: relevance for neuropsychiatric disorders. Behav Brain Res 198:83–90. doi:10.1016/j.bbr.2008.10.018
30. Delic S, Streif S, Deussing JM et al (2008) Genetic mouse models for behavioral analysis through transgenic RNAi technology. Genes, Brain Behav 7:821–830. doi:10.1111/j.1601-183X.2008.00412.x
31. Sperlágh B, Illes P (2014) P2X7 receptor: an emerging target in central nervous system diseases. Trends Pharmacol Sci 35:537–547. doi:10.1016/j.tips.2014.08.002
32. Bartlett R, Stokes L, Sluyter R (2014) The P2X7 Receptor Channel: recent developments and the use of P2X7 antagonists in models of disease. Pharmacol Rev 66:638–675. doi:10.1124/pr.113.008003
33. Aprile-Garcia F, Metzger MW, Paez-Pereda M et al (2016) Co-expression of wild-type P2X7R with Gln460Arg variant alters receptor function. PLoS One 11(3):e0151862. doi:10.1371/journal.pone.0151862
34. Stokes L, Fuller SJ, Sluyter R et al (2010) Two haplotypes of the P2X(7) receptor containing the Ala-348 to Thr polymorphism exhibit a gain-of-function effect and enhanced interleukin-1beta secretion. FASEB J 24:2916–2927. doi:10.1096/fj.09-150862
35. Rodríguez CI, Buchholz F, Galloway J et al (2000) High-efficiency deleter mice show that FLPe is an alternative to cre-loxP. Nat Genet 25:139–140. doi:10.1038/75973
36. Tronche F, Kellendonk C, Kretz O et al (1999) Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat Genet 23:99–103. doi:10.1038/12703
37. Goebbels S, Bormuth I, Bode U et al (2006) Genetic targeting of principal neurons in neocortex and hippocampus of NEX-cre mice. Genesis 44:611–621. doi:10.1002/dvg.20256
38. Monory K, Massa F, Egertová M et al (2006) The Endocannabinoid system controls key epileptogenic circuits in the hippocampus. Neuron 51:455–466. doi:10.1016/j.neuron.2006.07.006
39. Mori T, Tanaka K, Buffo A et al (2006) Inducible gene deletion in astroglia and radial glia - a valuable tool for functional and lineage analysis. Glia 54:21–34. doi:10.1002/glia
40. Lappe-Siefke C, Goebbels S, Gravel M et al (2003) Disruption of Cnp1 uncouples oligodendroglial functions in axonal support and myelination. Nat Genet 33:366–374. doi:10.1038/ng1095
41. Parkhurst CN, Yang G, Ninan I et al (2013) Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor. Cell 155:1596–1609. doi:10.1016/j.cell.2013.11.030
42. Kimmel RA, Turnbull DH, Blanquet V et al (2000) Two lineage boundaries coordinate vertebrate apical ectodermal ridge formation. Genes Dev 14:1377–1389. doi:10.1101/gad.14.11.1377
43. Aller MI, Jones A, Merlo D et al (2003) Cerebellar granule cell Cre recombinase expression. Genesis 36:97–103. doi:10.1002/gene.10204
44. Bender J, Engeholm M, Ederer MS et al (2015) Corticotropin-releasing hormone receptor type 1 (CRHR1) clustering with MAGUKs is mediated via its C-terminal PDZ binding motif. PLoS One 10:1–23. doi:10.1371/journal.pone.0136768
45. Allen JW, Mutkus LA, Aschner M (2001) Isolation of neonatal rat cortical astrocytes for primary cultures. In: Maines M, Costa LG, Sipes GI (eds) Current protocols in toxicology. John Wiley and Sons, New York, pp 12.4.1–12.4.15
46. Saura J, Tusell JM, Serratosa J (2003) High-yield isolation of murine microglia by mild Trypsinization. Glia 44:183–189. doi:10.1002/glia.10274
47. Yona S, Kim K-W, Wolf Y et al (2013) Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity 38:79–91. doi:10.1016/j.immuni.2012.12.001.Fate
48. Lucae S, Salyakina D, Barden N et al (2006) P2RX7, a gene coding for a purinergic ligand-gated ion channel, is associated with major depressive disorder. Hum Mol Genet 15:2438–2445. doi:10.1093/hmg/ddl166
49. Barden N, Harvey M, Gagné B et al (2006) Analysis of single nucleotide polymorphisms in genes in the chromosome 12Q24.31 region points to P2RX7 as a susceptibility gene to bipolar affective disorder. Am J Med Genet B Neuropsychiatr Genet 141B:374–382. doi:10.1002/ajmg.b.30303
50. Sluyter R, Stokes L (2011) Significance of P2X7 receptor variants to human health and disease. Recent Pat DNA Gene Seq 5:41–54
51. Soltoff SP, McMillian MK, Talamo BR (1989) Coomassie brilliant blue G is a more potent antagonist of P2 purinergic responses than reactive blue 2 (Cibacron blue 3GA) in rat parotid acinar cells. Biochem Biophys Res Commun 165:1279–1285. doi:10.1016/0006-291X(89)92741-1
52. Lambrecht G, Friebe T, Grimm U et al (1992) PPADS, a novel functionally selective antagonist of P2 purinoceptor-mediated responses. Eur J Pharmacol 217:217–219. doi:10.1016/0014-2999(92)90877-7
53. Qiu F, Dahl G (2009) A permeant regulating its permeation pore: inhibition of pannexin 1 channels by ATP. Am J Physiol Cell Physiol 296:C250–C255. doi:10.1152/ajpcell.00433.2008
54. Nicke A, Bäumert HG, Rettinger J et al (1998) P2X1 and P2X3 receptors form stable trimers: a novel structural motif of ligand-gated ion channels. EMBO J 17:3016–3028. doi:10.1093/emboj/17.11.3016
55. North RA, Jarvis MF (2013) P2X receptors as drug targets. Mol Pharmacol 83:759–769. doi:10.1124/mol.112.083758
56. Chrovian CC, Rech JC, Bhattacharya A, Letavic MA (2014) P2X7 antagonists as potential therapeutic agents for the treatment of CNS disorders. Prog Med Chem 53:65–100. doi:10.1016/B978-0-444-63380-4.00002-0
57. Nörenberg W, Hempel C, Urban N et al (2011) Clemastine potentiates the human P2X7 receptor by sensitizing it to lower ATP concentrations. J Biol Chem 286:11067–11081. doi:10.1074/jbc.M110.198879
58. Fischer W, Urban N, Immig K et al (2014) Natural compounds with P2X7 receptor-modulating properties. Purinergic Signal 10:313–326. doi:10.1007/s11302-013-9392-1
59. Khakh BS, North RA (2012) Neuromodulation by extracellular ATP and P2X receptors in the CNS. Neuron 76:51–69. doi:10.1016/j.neuron.2012.09.024
60. Guo C, Masin M, Qureshi OS, Murrell-Lagnado RD (2007) Evidence for functional P2X4/P2X7 heteromeric receptors. Mol Pharmacol 72:1447–1456. doi:10.1124/mol.107.035980
61. Antonio LS, Stewart AP, Xu XJ et al (2011) P2X4 receptors interact with both P2X2 and P2X7 receptors in the form of homotrimers. Br J Pharmacol 163:1069–1077. doi:10.1111/j.1476-5381.2011.01303.x
62. Franke H, Illes P (2006) Involvement of P2 receptors in the growth and survival of neurons in the CNS. Pharmacol Ther 109:297–324. doi:10.1016/j.pharmthera.2005.06.002
63. Deussing JM (2013) Targeted mutagenesis tools for modelling psychiatric disorders. Cell Tissue Res 354:9–25. doi:10.1007/s00441-013-1708-5
64. García-Huerta P, Díaz-Hernandez M, Delicado EG et al (2012) The specificity protein factor Sp1 mediates transcriptional regulation of P2X7 receptors in the nervous system. J Biol Chem 287:44628–44644. doi:10.1074/jbc.M112.390971
65. Jimenez-Mateos EM, Arribas-Blazquez M, Sanz-Rodriguez A et al (2015) microRNA targeting of the P2X7 purinoceptor opposes a contralateral epileptogenic focus in the hippocampus. Sci Rep 5:17486. doi:10.1038/srep17486
66. Hirayama Y, Ikeda-Matsuo Y, Notomi S et al (2015) Astrocyte-mediated ischemic tolerance. J Neurosci 35:3794–3805. doi:10.1523/JNEUROSCI.4218-14.2015
67. Lammel S, Steinberg EE, Földy C et al (2015) Diversity of transgenic mouse models for selective targeting of midbrain dopamine neurons. Neuron 85:429–438. doi:10.1016/j.neuron.2014.12.036
68. Chen Y, Molet J, Gunn BG et al (2015) Diversity of reporter expression patterns in transgenic mouse lines targeting corticotropin- releasing hormone-expressing neurons. Endocrinology 156:4769–4780. doi:10.1210/en.2015-1673