Cannabinoid receptor-2 stimulation suppresses neuroinflammation by regulating microglial M1/M2 polarization through the cAMP/PKA pathway in an experimental GMH rat model

Brain, Behavior, and Immunity

Volumn 58, Issue , 2016, Pages 118-129

  Tao, Yihao ^a   Li, Lin ^b   Jiang, Bing ^a   Feng, Zhou ^a   Yang, Liming ^a   Tang, Jun ^a   Chen, Qianwei ^a   Zhang, Jianbo ^a   Tan, Qiang ^a   Feng, Hua ^a   Chen, Zhi ^a   Zhu, Gang ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

^b Nanchong Central Hospital   (China)

Author keywords

Anti inflammation; Cannabinoid receptor 2; Microglial polarization; PKA

Indexed keywords

1 DEOXY 3 (1,1 DIMETHYLBUTYL) DELTA8 TETRAHYDROCANNABINOL; CANNABINOID 2 RECEPTOR; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; EPAC1 PROTEIN; MEMBRANE PROTEIN; THROMBIN; UNCLASSIFIED DRUG; CYTOKINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN HEMORRHAGE; CELL TRANSFORMATION; CONTROLLED STUDY; CYTOKINE RELEASE; DRUG MECHANISM; GERMINAL MATRIX HEMORRHAGE; MACROPHAGE; MALE; MICROGLIA; NERVOUS SYSTEM INFLAMMATION; NEWBORN; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; ANIMAL; CELL POLARITY; DISEASE MODEL; ENCEPHALITIS; IMMUNOLOGY; METABOLISM; SPRAGUE DAWLEY RAT;

ANIMALS; CELL POLARITY; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYTOKINES; DISEASE MODELS, ANIMAL; ENCEPHALITIS; INTRACRANIAL HEMORRHAGES; MALE; MICROGLIA; RATS, SPRAGUE-DAWLEY; RECEPTOR, CANNABINOID, CB2; SIGNAL TRANSDUCTION;

EID: 84973575200     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2016.05.020     Document Type: Article

References (53)

1. Adams, J.A., McGlone, M.L., Gibson, R., Taylor, S.S., Phosphorylation modulates catalytic function and regulation in the cAMP-dependent protein kinase. Biochemistry 34 (1995), 2447–2454.
2. Aronoff, D.M., Carstens, J.K., Chen, G.H., Toews, G.B., Peters-Golden, M., Short communication: differences between macrophages and dendritic cells in the cyclic AMP-dependent regulation of lipopolysaccharide-induced cytokine and chemokine synthesis. J. Interferon Cytokine Res. 26 (2006), 827–833.
3. Aronowski, J., Zhao, X., Molecular pathophysiology of cerebral hemorrhage: secondary brain injury. Stroke 42 (2011), 1781–1786.
4. Ashton, J.C., Glass, M., The cannabinoid CB2 receptor as a target for inflammation-dependent neurodegeneration. Curr. Neuropharmacol. 5 (2007), 73–80.
5. Ballabh, P., Intraventricular hemorrhage in premature infants: mechanism of disease. Pediatr. Res. 67 (2010), 1–8.
6. Ballabh, P., Pathogenesis and prevention of intraventricular hemorrhage. Clin. Perinatol. 41 (2014), 47–67.
7. Beavo, J.A., Brunton, L.L., Cyclic nucleotide research – still expanding after half a century. Nat. Rev. Mol. Cell Biol. 3 (2002), 710–718.
8. Borner, C., Smida, M., Hollt, V., Schraven, B., Kraus, J., Cannabinoid receptor type 1- and 2-mediated increase in cyclic AMP inhibits T cell receptor-triggered signaling. J. Biol. Chem. 284 (2009), 35450–35460.
9. Cabral, G.A., Raborn, E.S., Griffin, L., Dennis, J., Marciano-Cabral, F., CB2 receptors in the brain: role in central immune function. Br. J. Pharmacol. 153 (2008), 240–251.
10. Chhor, V., Le Charpentier, T., Lebon, S., Ore, M.V., Celador, I.L., Josserand, J., Degos, V., Jacotot, E., Hagberg, H., Savman, K., Mallard, C., Gressens, P., Fleiss, B., Characterization of phenotype markers and neuronotoxic potential of polarised primary microglia in vitro. Brain Behav. Immun. 32 (2013), 70–85.
11. Chin, K.V., Yang, W.L., Ravatn, R., Kita, T., Reitman, E., Vettori, D., Cvijic, M.E., Shin, M., Iacono, L., Reinventing the wheel of cyclic AMP: novel mechanisms of cAMP signaling. Ann. N. Y. Acad. Sci. 968 (2002), 49–64.
12. David, S., Kroner, A., Repertoire of microglial and macrophage responses after spinal cord injury. Nat. Rev. Neurosci. 12 (2011), 388–399.
13. Deren, K.E., Packer, M., Forsyth, J., Milash, B., Abdullah, O.M., Hsu, E.W., McAllister, J.P. 2nd., Reactive astrocytosis, microgliosis and inflammation in rats with neonatal hydrocephalus. Exp. Neurol. 226 (2010), 110–119.
14. Ehrhart, J., Obregon, D., Mori, T., Hou, H., Sun, N., Bai, Y., Klein, T., Fernandez, F., Tan, J., Shytle, R.D., Stimulation of cannabinoid receptor 2 (CB2) suppresses microglial activation. J. Neuroinflammation, 2, 2005, 29.
15. Fernandez-Ruiz, J., Pazos, M.R., Garcia-Arencibia, M., Sagredo, O., Ramos, J.A., Role of CB2 receptors in neuroprotective effects of cannabinoids. Mol. Cell. Endocrinol. 286 (2008), S91–S96.
16. Fujii, M., Sherchan, P., Soejima, Y., Hasegawa, Y., Flores, J., Doycheva, D., Zhang, J.H., Cannabinoid receptor type 2 agonist attenuates apoptosis by activation of phosphorylated CREB-Bcl-2 pathway after subarachnoid hemorrhage in rats. Exp. Neurol. 261 (2014), 396–403.
17. Ghosh, M., Garcia-Castillo, D., Aguirre, V., Golshani, R., Atkins, C.M., Bramlett, H.M., Dietrich, W.D., Pearse, D.D., Proinflammatory cytokine regulation of cyclic AMP-phosphodiesterase 4 signaling in microglia in vitro and following CNS injury. Glia 60 (2012), 1839–1859.
18. Ghosh, M., Xu, Y., Pearse, D.D., Cyclic AMP is a key regulator of M1 to M2a phenotypic conversion of microglia in the presence of Th2 cytokines. J. Neuroinflammation, 13, 2016, 9.
19. Gong, B., Shelite, T., Mei, F.C., Ha, T., Hu, Y., Xu, G., Chang, Q., Wakamiya, M., Ksiazek, T.G., Boor, P.J., Bouyer, D.H., Popov, V.L., Chen, J., Walker, D.H., Cheng, X., Exchange protein directly activated by cAMP plays a critical role in bacterial invasion during fatal rickettsioses. Proc. Natl. Acad. Sci. USA 110 (2013), 19615–19620.
20. Gordon, S., Alternative activation of macrophages. Nat. Rev. Immunol. 3 (2003), 23–35.
21. Grandoch, M., Roscioni, S.S., Schmidt, M., The role of Epac proteins, novel cAMP mediators, in the regulation of immune, lung and neuronal function. Br. J. Pharmacol. 159 (2010), 265–284.
22. Hanisch, U.K., Kettenmann, H., Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat. Neurosci. 10 (2007), 1387–1394.
23. Iadecola, C., Anrather, J., The immunology of stroke: from mechanisms to translation. Nat. Med. 17 (2011), 796–808.
24. Lekic, T., Manaenko, A., Rolland, W., Krafft, P.R., Peters, R., Hartman, R.E., Altay, O., Tang, J., Zhang, J.H., Rodent neonatal germinal matrix hemorrhage mimics the human brain injury, neurological consequences, and post-hemorrhagic hydrocephalus. Exp. Neurol. 236 (2012), 69–78.
25. Logue, J.S., Scott, J.D., Organizing signal transduction through A-kinase anchoring proteins (AKAPs). FEBS J. 277 (2010), 4370–4375.
26. Luo, M., Jones, S.M., Phare, S.M., Coffey, M.J., Peters-Golden, M., Brock, T.G., Protein kinase A inhibits leukotriene synthesis by phosphorylation of 5-lipoxygenase on serine 523. J. Biol. Chem. 279 (2004), 41512–41520.
27. Mecha, M., Iñigo, P.M., Mestre, L., Hernangómez, M., Borrell, J., Guaza, C., An easy and fast way to obtain a high number of glial cells from rat cerebral tissue: a beginners approach. Protocol Exch., 2011, 10.1038/protex.2011.218.
28. Mecha, M., Feliu, A., Carrillo-Salinas, F.J., Rueda-Zubiaurre, A., Ortega-Gutierrez, S., de Sola, R.G., Guaza, C., Endocannabinoids drive the acquisition of an alternative phenotype in microglia. Brain Behav. Immun. 49 (2015), 233–245.
29. Miller, A.M., Stella, N., CB2 receptor-mediated migration of immune cells: it can go either way. Br. J. Pharmacol. 153 (2008), 299–308.
30. Moller, T., Hanisch, U.K., Ransom, B.R., Thrombin-induced activation of cultured rodent microglia. J. Neurochem. 75 (2000), 1539–1547.
31. Nevo, I., Avidor-Reiss, T., Levy, R., Bayewitch, M., Heldman, E., Vogel, Z., Regulation of adenylyl cyclase isozymes on acute and chronic activation of inhibitory receptors. Mol. Pharmacol. 54 (1998), 419–426.
32. Ohnishi, M., Katsuki, H., Fujimoto, S., Takagi, M., Kume, T., Akaike, A., Involvement of thrombin and mitogen-activated protein kinase pathways in hemorrhagic brain injury. Exp. Neurol. 206 (2007), 43–52.
33. Pan, J., Jin, J.L., Ge, H.M., Yin, K.L., Chen, X., Han, L.J., Chen, Y., Qian, L., Li, X.X., Xu, Y., Malibatol A regulates microglia M1/M2 polarization in experimental stroke in a PPARgamma-dependent manner. J. Neuroinflammation, 12, 2015, 51.
34. Pandya, C.D., Kutiyanawalla, A., Pillai, A., BDNF-TrkB signaling and neuroprotection in schizophrenia. Asian J. Psychiatry 6 (2013), 22–28.
35. Patrizio, M., Tumor necrosis factor reduces cAMP production in rat microglia. Glia 48 (2004), 241–249.
36. Pearse, D.D., Pereira, F.C., Marcillo, A.E., Bates, M.L., Berrocal, Y.A., Filbin, M.T., Bunge, M.B., CAMP and Schwann cells promote axonal growth and functional recovery after spinal cord injury. Nat. Med. 10 (2004), 610–616.
37. Seino, S., Shibasaki, T., PKA-dependent and PKA-independent pathways for cAMP-regulated exocytosis. Physiol. Rev. 85 (2005), 1303–1342.
38. Sheldon, K.E., Shandilya, H., Kepka-Lenhart, D., Poljakovic, M., Ghosh, A., Morris, S.M. Jr., Shaping the murine macrophage phenotype: IL-4 and cyclic AMP synergistically activate the arginase I promoter. J. Immunol. 191 (2013), 2290–2298.
39. Shennan, A.H., Bewley, S., Why should preterm births be rising?. BMJ 332 (2006), 924–925.
40. Strahle, J., Garton, H.J., Maher, C.O., Muraszko, K.M., Keep, R.F., Xi, G., Mechanisms of hydrocephalus after neonatal and adult intraventricular hemorrhage. Transl. Stroke Res. 3 (2012), 25–38.
41. Tang, J., Tao, Y., Tan, L., Yang, L., Niu, Y., Chen, Q., Yang, Y., Feng, H., Chen, Z., Zhu, G., Cannabinoid receptor 2 attenuates microglial accumulation and brain injury following germinal matrix hemorrhage via ERK dephosphorylation in vivo and in vitro. Neuropharmacology 95 (2015), 424–433.
42. Tang, J., Chen, Q., Guo, J., Yang, L., Tao, Y., Li, L., Miao, H., Feng, H., Chen, Z., Zhu, G., Minocycline attenuates neonatal germinal-matrix-hemorrhage-induced neuroinflammation and brain edema by activating cannabinoid receptor 2. Mol. Neurobiol. 53 (2016), 1935–1948.
43. Tang, J., Tao, Y., Jiang, B., Chen, Q., Hua, F., Zhang, J., Zhu, G., Chen, Z., Pharmacological preventions of brain injury following experimental germinal matrix hemorrhage: an up-to-date review. Transl. Stroke Res. 7 (2016), 20–32.
44. Tao, Y., Tang, J., Chen, Q., Guo, J., Li, L., Yang, L., Feng, H., Zhu, G., Chen, Z., Cannabinoid CB2 receptor stimulation attenuates brain edema and neurological deficits in a germinal matrix hemorrhage rat model. Brain Res. 1602 (2015), 127–135.
45. Walter, L., Franklin, A., Witting, A., Wade, C., Xie, Y., Kunos, G., Mackie, K., Stella, N., Nonpsychotropic cannabinoid receptors regulate microglial cell migration. J. Neurosci. 23 (2003), 1398–1405.
46. Wang, G., Shi, Y., Jiang, X., Leak, R.K., Hu, X., Wu, Y., Pu, H., Li, W.W., Tang, B., Wang, Y., Gao, Y., Zheng, P., Bennett, M.V., Chen, J., HDAC inhibition prevents white matter injury by modulating microglia/macrophage polarization through the GSK3beta/PTEN/Akt axis. Proc. Natl. Acad. Sci. USA 112 (2015), 2853–2858.
47. Xi, G., Reiser, G., Keep, R.F., The role of thrombin and thrombin receptors in ischemic, hemorrhagic and traumatic brain injury: deleterious or protective?. J. Neurochem. 84 (2003), 3–9.
48. Xi, G., Keep, R.F., Hoff, J.T., Mechanisms of brain injury after intracerebral haemorrhage. Lancet Neurol. 5 (2006), 53–63.
49. Xu, Y., Xu, Y., Wang, Y., Wang, Y., He, L., Jiang, Z., Huang, Z., Liao, H., Li, J., Saavedra, J.M., Zhang, L., Pang, T., Telmisartan prevention of LPS-induced microglia activation involves M2 microglia polarization via CaMKKbeta-dependent AMPK activation. Brain Behav. Immun. 50 (2015), 298–313.
50. Yang, Y., Salayandia, V.M., Thompson, J.F., Yang, L.Y., Estrada, E.Y., Yang, Y., Attenuation of acute stroke injury in rat brain by minocycline promotes blood-brain barrier remodeling and alternative microglia/macrophage activation during recovery. J. Neuroinflammation, 12, 2015, 26.
51. Zarruk, J.G., Fernandez-Lopez, D., Garcia-Yebenes, I., Garcia-Gutierrez, M.S., Vivancos, J., Nombela, F., Torres, M., Burguete, M.C., Manzanares, J., Lizasoain, I., Moro, M.A., Cannabinoid type 2 receptor activation downregulates stroke-induced classic and alternative brain macrophage/microglial activation concomitant to neuroprotection. Stroke 43 (2012), 211–219.
52. Zhang, Y., Lv, X., Bai, Y., Zhu, X., Wu, X., Chao, J., Duan, M., Buch, S., Chen, L., Yao, H., Involvement of sigma-1 receptor in astrocyte activation induced by methamphetamine via up-regulation of its own expression. J. Neuroinflammation, 12, 2015, 29.
53. Zhou, Y., Wang, Y., Wang, J., Anne Stetler, R., Yang, Q.W., Inflammation in intracerebral hemorrhage: from mechanisms to clinical translation. Prog. Neurobiol. 115 (2014), 25–44.