Δ9-THC and N-arachidonoyl glycine regulate BV-2 microglial morphology and cytokine release plasticity: Implications for signaling at GPR18

Frontiers in Pharmacology

Volumn 4 JAN, Issue , 2014, Pages

  McHugh, Douglas ^a,b   Roskowski, Daniel ^a   Xie, Sisi ^a   Bradshaw, Heather B ^a  

^a INDIANA UNIVERSITY   (United States)

^b New York   (United States)

Author keywords

BV 2; Cytokine; GPR18; Microglia; Morphology; NAGly; Phenotype

Indexed keywords

AXL PROTEIN; CANNABIDIOL; CD40 ANTIGEN; CELL PROTEIN; CYTOKINE; DRONABINOL; GELATINASE B; GLYCINE; N ARACHIDONOYL GLYCINE; OSTEOPONTIN; PROTEIN GPR18; SOMATOMEDIN C; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL COMMUNICATION; CELL INTERACTION; CELL PROLIFERATION; CELL STRUCTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENZYME LINKED IMMUNOSORBENT ASSAY; LONG TERM EXPOSURE; MICROARRAY ANALYSIS; MICROGLIA; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

EID: 84893767756     PISSN: None     EISSN: 16639812     Source Type: Journal    
DOI: 10.3389/fphar.2013.00162     Document Type: Article

References (44)

1. Begg, M., Pacher, P., Bátkai, S., Osei-Hyiaman, D., Offertáler, L., Mo, F. M., et al. (2005). Evidence for novel cannabinoid receptors. Pharmacol. Ther. 106,133-145. doi: 10.1016/j.pharmthera.2004.11.005.
2. Blasi, E., Barluzzi, R., Bocchini, V., Mazzolla, R., and Bistoni, F. (1990). Immortalization of murine microglial cells by a v-raf/v-myc carrying retrovirus. J. Neuroimmunol. 27, 229-237. doi: 10.1016/0165-5728(90)90073-V.
3. Block, M. L., Zecca, L., and Hong, J.-S. (2007). Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat. Rev. Neurosci. 8, 57-69. doi: 10.1038/nrn2038.
4. Bradshaw, H., Rimmerman, N., Hu, S., Benton, V., Stuart, J., Masuda, K., et al. (2009). The endocannabinoid anandamide is a precursor for the signaling lipid N-arachidonoyl glycine by two distinct pathways. BMC Biochem. 10:14. doi: 10.1186/1471-2091-10-14.
5. Cao, L., Plamer, C. D., Malon, J. T., and De Leo, J. A. (2009). Critical role of microglial CD40 in the maintenance of mechanical hypersensitivity in a murine model of neuropathic pain. Eur. J. Immunol. 39, 3562-3569. doi: 10.1002/eji.200939657.
6. Carson, M. J. (2002). Microglia as liaisons between the immune and central nervous systems: functional implications for multiple sclerosis. Glia 40, 218-231. doi: 10.1002/glia.10145.
7. Chatzigeorgious, A., Lyberi, M., Chatzilymperis, G., Nezos, A., and Kamper, E. (2009). CD40/CD40: signaling and its implications in health and disease. BioFactors 35, 474-483. doi: 10.1002/biof.62.
8. Colton, C., and Wilcock, D. (2010). Assessing activation states in microglia. CNS Neurol. Disord. Drug. Targets 9, 174-191. doi: 10.2174/187152710791012053.
9. Danton, G. H., and Dietrich, W. D. (2003). Inflammatory mechanisms after ischemia and stroke. J. Neuropathol. Exp. Neurol. 62,127-136.
10. Eikelenboom, P., Bate, C., Van Gool, W. A., Hoozemans, J. J., Rozemuller. J. M., Veerhuis, R., et al. (2002). Neuroinflammation in Alzheimer's disease and prion disease. Glia 40, 232-239. doi: 10.1002/glia.10146.
11. Fetler, L., and Amigorena, S. (2005). Neuroscience. Brain under surveillance: the microglia patrol. Science 309, 392-393. doi: 10.1126/science.1114852.
12. Fontainhas, A. M., Wang, M., Liang, K. J., Chen, S., Mettu, P., Damani, M., et al. (2011). Microglial morphology and dynamic behavior is regulated by ionotropic glutamatergic and GABAergic neurotransmission. PLoS ONE 6:e15973. doi: 10.1371/journal.pone.0015973.
13. Gallagher, E. J., Fierz, Y., Ferguson, R. D., and LeRoith, D. (2010). The pathway from diabetes and obesity to cancer, on the route to targeted therapy. Endocr. Pract. 16, 864-873. doi: 10.4158/EP10098.RA.
14. Gantz, I., Muraoka, A., Yang, Y.-K., Samuelson, L. C., Zimmerman, E. M., and Cook, H. et al. (1997). Cloning and chromosomal localization of a gene (GPR18) encoding a novel seven transmembrane receptor highly expressed in spleen and testis. Genomics 42, 462-466. doi: 10.1006/geno.1997.4752.
15. Garden, G. A., and Moller, T. (2006). Microglia biology in health and disease. J Neuroimmune Pharmacol. 1, 127-137. doi: 10.1007/s11481-006-9015-5.
16. Gordon, S. (2003). Alternative activation of macrophages. Nat. Rev. Immunol. 3, 23-35. doi: 10.1038/nri978.
17. Heide, I., Sokoll, A. C., Henz, B. M., Nagel, S., Kreissig, K., Grützkau, A., et al. (1998). Regulation and possible function of axl expression in immature human mast cells. Ann. Hematol. 77, 199-205. doi: 10.1007/s002770050443.
18. Járai, Z., Wagner, J. A., Varga, K. R., Lake, K. D., Compton, D. R., Martin, B. R., et al. (1999). Cannabinoid-induced mesenteric vasodilation through an endothelial site distinct from CB1 or CB2 receptors. Proc. Natl. Acad. Sci. U.S.A. 96, 14136-14141. doi: 10.1073/pnas.96.24.14136.
19. Ji, K., Akgul, G., Wollmuth, L. P., and Tsirka, S. E. (2013). Microglia actively regulate the number of functional synapses. PLoS ONE 8:e56293. doi:10.1371/journal.pone.0056293.
20. Jones, J. I., and Clemmons, D. R. (1995). Insulin-like growth factors and their binding proteins: biological actions. Endocr. Rev. 16, 3-34.
21. Kähäri, V.-M., and Saariaho-Kere, U. (1997). Matrix metalloproteinases in skin. Exp. Dermatol. 6, 199-213. doi: 10.1111/j.1600-0625.1997.tb00164.x.
22. Kohno, M., Hasegawa, H., Inoue, A., Muraoka, M., Miyazaki, T., Oka, K., et al. (2006). Identification of N-arachidonylglycine as the endogenous ligand for orphan G-protein-coupled receptor GPR18. Biochem. Biophyl. Res. Comm. 347, 827-832. doi: 10.1016/j.bbrc.2006.06.175.
23. Mackie, K., and Stella, N. (2006). Cannabinoid receptors and endocannabinoids: Evidence for new players. AAPS J. 8, E298-E306.
24. Mark, M. R., Chen, J., Hammonds, R. G., Sadick, M., and Godowsk, P. J. (1996). Characterization of Gas6, a member of the superfamily of G domain-containing proteins, as a ligand for Rse and Axl. J. Biol. Chem. 271, 9785-9789. doi: 10.1074/jbc.271.16.9785.
25. Mazzali, M., Kipari, T., Ophascharoensuk, V., Wesson, J. A., Johnson, R., and Hughes, J. (2002). Osteopontin-a molecule or all seasons. Q. J. Med. 95, 3-13. doi: 10.1093/qjmed/95.1.3.
26. McHugh, D., Hu, S. S.-J., Rimmerman, N., Juknat, A., Vogel, Z., Walker, J. M., et al. (2010). N-arachidonoyl glycine, an abundant endogenous lipid, potently drives directed cellular migration through GPR18, the putative abnormal cannabidiol receptor. BMC Neurosci. 11:44. doi: 10.1186/1471-2202-11-44.
27. McHugh, D. (2012). GPR18 in microglia: implications for the CNS and endocannabinoid system signalling. Br. J. Pharmacol. 167, 1575-1582. doi: 10.1111/j.1476-5381.2012.02019.x.
28. McHugh, D., Page, J., Dunn, E., and Bradshaw, H. B. (2012a). (9-THC and N-arachidonoyl glycine are full agonists at GPR18 and cause migration in the human endometrial cell line, HEC-1B. Br. J. Pharmacol. 165, 2414-2424. doi: 10.1111/j.1476-5381.2011.01497.x.
29. McHugh, D., Wager-Miller, J., Page, J., and Bradshaw, H. B. (2012b). siRNA knockdown of GPR18 receptors in BV-2 microglia attenuates the cell migration induced by N-arachidonyl glycine. J. Mol. Signal. 7, 10. doi: 10.1186/1750-2187-7-10.
30. Oh, D. Y., Yoon, J. M., Moon, M. J., Hwang, J. I., Choe, H., Lee, J. Y., et al. (2008). Identification of farnesyl pyrophosphate and N-arachidonylglycine as endogenous ligands for GPR92. J. Biol. Chem. 283, 21054-21064. doi: 10.1074/jbc.M708908200.
31. Pertwee, R. G., Howlett, A. C., Abood, M. E., Alexander, S. P. H., Di Marzo, V., Elphick, M. R. et al. (2010). International union of basic and clinical pharmacology. LXXIX. Cannabinoid receptors and their ligands: beyond CB1 and CB2. Pharmacol. Rev. 62, 588-631. doi: 10.1124/pr.110.003004.
32. Pöttler, M., Zierler, S., and Kerschbaum, H. H. (2006). An artificial three-dimensional matrix promotes ramification in the microglial cell-line, BV-2. Neurosci. Lett. 410, 137-140. doi: 10.1016/j.neulet.2006.09.082.
33. Qin, Y., Verdegaal, E. M. E., Siderius, M., Bebelman, J. P., Smit, M. J., and Leurs, R., et al. (2010). Quantitative expression profiling of G-protein-coupled receptors (GPCRs) in metastatic melanoma: the constitutively active orphan GPCR GPR18 as novel drug target. Pigment Cell Melanoma Res. 24, 207-218. doi: 10.1111/j.1755-148X.2010.00781.x.
34. Raivich, G. (2005). Like cops on the beat: the active role of resting microglia. Trends Neurosci. 28, 571-573. doi: 10.1016/j.tins.2005.09.001.
35. Sensi, M., Catani, M., Castellano, G., Nicolini, G., Alciato, F., Tragni, G., et al. (2011). Human cutaneous melanomas lacking MITF and melanocyte differentiation antigens express a functional Axl receptor kinase. J. Invest. Dermatol. 131, 2448-2457. doi: 10.1038/jid.2011.218.
36. Streit, W. J. (2002). Microglia as neuroprotective, immunocompetent cells of the CNS. Glia 40, 133-139. doi: 10.1002/glia.10154.
37. Tan, J., Town, T., Crawford, F., Mori, T., DelleDonne, A., Crescentini, R., et al. (2002). Role of CD40 ligand in amyloidosis in transgenic Alzheimer's mice. Nat. Neurosci. 5, 1288-1293. doi: 10.1038/nn968.
38. Toth, M., Chvyrkova, I., Bernardo, M. M., Hernandez-Barrantes, S., and Fridman, R. (2003). Pro-MMP-9 activation by the MT1-MMP/MMP-2 axis and MMP-3: role of TIMP-2 and plasma membranes. Biochem. Biophys. Res. Commun. 308, 386-395. doi: 10.1016/S0006-291X(03)01405-0.
39. Tremblay, M. E., Lowery, R. L., and Majewska, A. K. (2010). Microglial interactions with synapses are modulated by visual experience. PLoS Biol. 8:e1000527. doi:10.1371/journal.pbio.1000527.
40. Ueno, M., Fujita, Y., Tanaka, T., Nakamura, Y., Kikuta, J., Ishii, M., et al. (2013). Layer V cortical neurons require microglial support for survival during postnatal development. Nat. Neurosci. 16, 543-551. doi: 10.1038/nn.3358.
41. van Rossum, D., and Hanisch, U-K. (2004). Microglia. Metab. Brain Dis. 19, 393-411. doi: 10.1023/B:MEBR.0000043984.73063.d8.
42. Walter, L., Franklin, A., Witting, A., Wade, C,. Xie, Y., Kunos, G., Mackie, K., and Stella, N. (2003). Nonpsychotropic cannabinoid receptors regulate microglial cell migration. J. Neurosci. 23, 1398-1405.
43. Wang, J., and Tsirka, S. E. (2005). Neuroprotection by inhibition of matrix metalloproteinases in a mouse model of intracerebral haemorrhage. Brain 128, 1622-1633. doi: 10.1093/brain/awh489.
44. Zhang, J., Geula, C., Lu, C., Koziel, H., Hatcher, L. M., Roisen, F. J. (2003). Neurotrophins regulate proliferation and survival of two microglial cell lines in vitro. Exp. Neurol. 183, 469-481. doi: 10.1016/S0014-4886(03)00222-X.