Microglial Kv1.3 Channels and P2Y12 receptors differentially regulate cytokine and chemokine release from brain slices of young adult and aged mice

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Charolidi, Nicoletta ^a   Schilling, Tom ^a   Eder, Claudia ^a  

^a ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE RECEPTOR; CHEMOKINE; CXCL1 CHEMOKINE; CYTOKINE; INTERLEUKIN 6; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR2.1; LIPOPOLYSACCHARIDE; MARGATOXIN; MONOCYTE CHEMOTACTIC PROTEIN 1; POTASSIUM CHANNEL KV1.3; PURINERGIC P2Y12 RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

ADULT; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INJURY; BRAIN SLICE; CELL STIMULATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; FEMALE; MICROGLIA; MOLECULAR MECHANICS; MOUSE; NONHUMAN; REGULATORY MECHANISM; TISSUE PREPARATION; YOUNG ADULT; AGING; ANIMAL; BIOLOGICAL MODEL; BRAIN; CYTOLOGY; GENE EXPRESSION REGULATION; IMMUNOLOGY; METABOLISM;

MUS;

AGING; ANIMALS; BRAIN; CHEMOKINES; CYTOKINES; GENE EXPRESSION REGULATION; KV1.3 POTASSIUM CHANNEL; LIPOPOLYSACCHARIDES; MICE; MICROGLIA; MODELS, BIOLOGICAL; RECEPTORS, PURINERGIC P2Y12;

EID: 84930225516     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0128463     Document Type: Article

References (43)

1. Lambertsen KL, Biber K, Finsen B. Inflammatory cytokines in experimental and human stroke. J Cereb Blood Flow Metab. 2012; 32: 1677-1698. doi: 10.1038/jcbfm.2012.88 PMID: 22739623
2. Taylor RA, Sansing LH. Microglial responses after ischemic stroke and intracerebral hemorrhage. Clin Dev Immunol 2013; 2013: 746068. doi: 10.1155/2013/746068 PMID: 24223607
3. Chen Y, Won SJ, Xu Y, Swanson RA. Targeting microglial activation in stroke therapy: pharmacological tools and gender effects. Curr Med Chem. 2014; 21: 2146-2155. PMID: 24372213
4. Benakis C, Garcia-Bonilla L, Iadecola C, Anrather J. The role of microglia and myeloid immune cells in acute cerebral ischemia. Front Cell Neurosci. 2015; 8: 461. doi: 10.3389/fncel.2014.00461 PMID: 25642168
5. Corps KN, Roth TL, McGavern DB. Inflammation and Neuroprotection in Traumatic Brain Injury. JAMA Neurol. 2015; 72: 355-362. doi: 10.1001/jamaneurol.2014.3558 PMID: 25599342
6. Kawabori M, Yenari MA. Inflammatory responses in Brain Ischemia. Curr Med Chem. 2015; 22: 1258-1277. PMID: 25666795
7. Melani A, Turchi D, Vannucchi MG, Cipriani S, Gianfriddo M, Pedata F. ATP extracellular concentrations are increased in the rat striatum during in vivo ischemia. Neurochem Int. 2005; 47: 442-448. PMID: 16029911
8. Haynes SE, Hollopeter G, Yang G, Kurpius D, Dailey ME, Gan WB, et al. The P2Y12 receptor regulates microglial activation by extracellular nucleotides. Nat Neurosci. 2006; 9: 1512-1519. PMID: 17115040
9. Orr AG, Orr AL, Li XJ, Gross RE, Traynelis SF. Adenosine A2A receptor mediates microglial process retraction. Nat Neurosci. 2009; 12: 872-878. doi: 10.1038/nn.2341 PMID: 19525944
10. Koizumi S, Shigemoto-Mogami Y, Nasu-Tada K, Shinozaki Y, Ohsawa K, Tsuda M, et al. UDP acting at P2Y6 receptors is a mediator of microglial phagocytosis. Nature. 2007; 446: 1091-1095. PMID: 17410128
11. Kim B, Jeong HK, Kim JH, Lee SY, Jou I, Joe EH. Uridine 5′-diphosphate induces chemokine expression in microglia and astrocytes through activation of the P2Y6 receptor. J Immunol. 2011; 186: 3701-3709. doi: 10.4049/jimmunol.1000212 PMID: 21317391
12. Nörenberg W, Gebicke-Haerter PJ, Illes P. Voltage-dependent potassium channels in activated rat microglia. J Physiol. 1994; 475: 15-32. PMID: 7514664
13. Schilling T, Eder C. Ion channel expression in resting and activated microglia of hippocampal slices from juvenile mice. Brain Res. 2007; 1186: 21-28. PMID: 18005942
14. Lyons SA, Pastor A, Ohlemeyer C, Kann O, Wiegand F, Prass K, et al. Distinct physiologic properties of microglia and blood-borne cells in rat brain slices after permanent middle cerebral artery occlusion. J Cereb Blood Flow Metab. 2000; 20: 1537-1549. PMID: 11083228
15. Menteyne A, Levavasseur F, Audinat E, Avignone E. Predominant functional expression of Kv1.3 by activated microglia of the hippocampus after Status epilepticus. PLOS ONE. 2009; 4(8): e6770. doi: 10.1371/journal.pone.0006770 PMID: 19707551
16. Peng Y, Lu K, Li Z, Zhao Y, Wang Y, Hu B, et al. Blockade of Kv1.3 channels ameliorates radiation-induced brain injury. Neuro Oncol. 2014; 16: 528-539. doi: 10.1093/neuonc/not221 PMID: 24305723
17. Rangaraju S, Gearing M, Jin LW, Levey A. Potassium channel Kv1.3 is highly expressed by microglia in human Alzheimer's disease. J Alzheimers Dis. 2015; 44: 797-808. doi: 10.3233/JAD-141704 PMID: 25362031
18. Butovsky O, Jedrychowski MP, Moore CS, Cialic R, Lanser AJ, Gabriely G, et al. Identification of a unique TGF-β-dependent molecular and functional signature in microglia. Nat Neurosci. 2014; 17:131-143. doi: 10.1038/nn.3599 PMID: 24316888
19. Orre M, Kamphuis W, Osborn LM, Melief J, Kooijman L, Huitinga I, et al. Acute isolation and transcriptome characterization of cortical astrocytes and microglia from young and aged mice. Neurobiol Aging. 2014; 35: 1-14. doi: 10.1016/j.neurobiolaging.2013.07.008 PMID: 23954174
20. Schilling T, Eder C. Microglial K+ channel expression in young adult and aged mice. Glia. 2015; 63: 664-672. doi: 10.1002/glia.22776 PMID: 25472417
21. Wong WT. Microglial aging in the healthy CNS: phenotypes, drivers, and rejuvenation. Front Cell Neurosci. 2013; 7: 22. doi: 10.3389/fncel.2013.00022 PMID: 23493481
22. Mosher KI, Wyss-Coray T. Microglial dysfunction in brain aging and Alzheimer's disease. Biochem Pharmacol. 2014; 88: 594-604. doi: 10.1016/j.bcp.2014.01.008 PMID: 24445162
23. Norden DM, Muccigrosso MM, Godbout JP. Microglial Priming and Enhanced Reactivity to Secondary Insult in Aging, and Traumatic CNS injury, and Neurodegenerative Disease. Neuropharmacology 2014; doi: 10.1016/j.neuropharm.2014.10.028. [Epub ahead of print]
24. Streit WJ, Xue QS. Human CNS immune senescence and neurodegeneration. Curr Opin Immunol 2014; 29: 93-96. doi: 10.1016/j.coi.2014.05.005 PMID: 24908174
25. Streit WJ, Xue QS, Tischer J, Bechmann I. Microglial pathology. Acta Neuropathol Commun. 2014; 2: 142. doi: 10.1186/s40478-014-0142-6 PMID: 25257319
26. Stoppini L, Buchs PA, Muller D. A simple method for organotypic cultures of nervous tissue. J Neurosci Methods. 1991; 37: 173-182. PMID: 1715499
27. Huuskonen J, Suuronen T, Miettinen R, van Groen T, Salminen A. A refined in vitro model to study inflammatory responses in organotypic membrane culture of postnatal rat hippocampal slices. J Neuroinflammation. 2005; 2: 25. PMID: 16285888
28. Quick ED, Leser JS, Clarke P, Tyler KL. Activation of intrinsic immune responses and microglial phagocytosis in an ex vivo spinal cord slice culture model of West Nile virus infection. J Virol. 2014; 88:13005-13014. doi: 10.1128/JVI.01994-14 PMID: 25165111
29. Wang HR, Wu M, Yu H, Long S, Stevens A, Engers DW, et al. Selective inhibition of the Kir2 family of inward rectifier potassium channels by a small molecule probe: the discovery, SAR, and pharmacological characterization of ML133. ACS Chem Biol. 2011; 6: 845-856. doi: 10.1021/cb200146a PMID: 21615117
30. Stence N, Waite M, Dailey ME. Dynamics of microglial activation: a confocal time-lapse analysis in hippocampal slices. Glia. 2001; 33: 256-266. PMID: 11241743
31. Ransohoff RM, Perry VH. Microglial physiology: unique stimuli, specialized responses. Annu Rev Immunol. 2009; 27: 119-145. doi: 10.1146/annurev.immunol.021908.132528 PMID: 19302036
32. Van Wagoner NJ, Oh JW, Repovic P, Benveniste EN. Interleukin-6 (IL-6) production by astrocytes: autocrine regulation by IL-6 and the soluble IL-6 receptor. J Neurosci. 1999; 19: 5236-5244. PMID: 10377335
33. Duque A, Gazula VR, Kaczmarek LK. Expression of Kv1.3 potassium channels regulates density of cortical interneurons. Dev Neurobiol. 2013; 73: 841-855. doi: 10.1002/dneu.22105 PMID: 23821603
34. Kumar A, Stoica BA, Sabirzhanov B, Burns MP, Faden AI, Loane DJ. Traumatic brain injury in aged animals increases lesion size and chronically alters microglial/macrophage classical and alternative activation states. Neurobiol Aging. 2013; 34: 1397-1411. doi: 10.1016/j.neurobiolaging.2012.11.013 PMID: 23273602
35. Kigerl KA, de Rivero Vaccari JP, Dietrich WD, Popovich PG, Keane RW. Pattern recognition receptors and central nervous system repair. Exp Neurol 2014; 258: 5-16. doi: 10.1016/j.expneurol.2014.01.001 PMID: 25017883
36. Sierra A, Gottfried-Blackmore AC, McEwen BS, Bulloch K. Microglia derived from aging mice exhibit an altered inflammatory profile. Glia. 2007; 55: 412-424. PMID: 17203473
37. Njie EG, Boelen E, Stassen FR, Steinbusch HW, Borchelt DR, Streit WJ. Ex vivo cultures of microglia from young and aged rodent brain reveal age-related changes in microglial function. Neurobiol Aging. 2012; 33: 195.e1-12.
38. Dissing-Olesen L, LeDue JM, Rungta RL, Hefendehl JK, Choi HB, MacVicar BA. Activation of neuronal NMDA receptors triggers transient ATP-mediated microglial process outgrowth. J Neurosci. 2014; 34: 10511-10527. doi: 10.1523/JNEUROSCI.0405-14.2014 PMID: 25100586
39. Eyo UB, Peng J, Swiatkowski P, Mukherjee A, Bispo A, Wu LJ. Neuronal hyperactivity recruits microglial processes via neuronal NMDA receptors and microglial P2Y12 receptors after status epilepticus. J Neurosci. 2014; 34: 10528-10540. doi: 10.1523/JNEUROSCI.0416-14.2014 PMID: 25100587
40. Jaerve A, Müller HW. Chemokines in CNS injury and repair. Cell Tissue Res. 2012; 349: 229-248. doi: 10.1007/s00441-012-1427-3 PMID: 22700007
41. Bartok A, Toth A, Somodi S, Szanto TG, Hajdu P, Panyi G, et al. Margatoxin is a non-selective inhibitor of human Kv1.3 K+ channels. Toxicon. 2014; 87: 6-16. doi: 10.1016/j.toxicon.2014.05.002 PMID: 24878374
42. Stock C, Schilling T, Schwab A, Eder C. Lysophosphatidylcholine stimulates IL-1β release from microglia via a P2X7 receptor-independent mechanism. J Immunol. 2006; 177: 8560-8568. PMID: 17142754
43. Eder C. Regulation of microglial behavior by ion channel activity. J Neurosci Res. 2005; 81: 314-321. PMID: 15929071