Anti-neuroinflammatory activity of a novel cannabinoid derivative by inhibiting the NF-κB signaling pathway in lipopolysaccharide-induced BV-2 microglial cells

Journal of Pharmacological Sciences

Volumn 121, Issue 2, 2013, Pages 119-130

  More, Sandeep Vasant ^a   Park, Ju Young ^b   Kim, Byung Wook ^a   Kumar, Hemant ^a   Lim, Hyung Woo ^a   Kang, Seong Mook ^a   Koppula, Sushruta ^a   Yoon, Sung Hwa ^b   Choi, Dong Kug ^a  

^a Konkuk University   (South Korea)

^b Ajou University   (South Korea)

Author keywords

Cannabinoid signaling; Lipopolysaccharide; Microglia; Neuroinflammation

Indexed keywords

CANNABINOID DERIVATIVE; CD 101; CYCLOOXYGENASE 2; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE P38; NITRIC OXIDE; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTI NEUROINFLAMMATORY ACTIVITY; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL ACTIVATION; CELL STIMULATION; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG POTENCY; DRUG SCREENING; DRUG STRUCTURE; DRUG SYNTHESIS; ENZYME PHOSPHORYLATION; GENE EXPRESSION; MEDIATOR RELEASE; MICROGLIA; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; SIGNAL TRANSDUCTION; UPREGULATION;

EID: 84874162831     PISSN: 13478613     EISSN: 13478648     Source Type: Journal    
DOI: 10.1254/jphs.12170FP     Document Type: Article

References (78)

1. Hirsch EC, Hunot S. Neuroinflammation in parkinson's disease: a target for neuroprotection? Lancet Neurol. 2009;8:382-397.
2. Maccioni RB, Rojo LE, Fernandez JA, Kuljis RO. The role of neuroimmunomodulation in alzheimer's disease. Ann N Y Acad Sci. 2009;1153:240-246.
3. Grigoriadis N, Grigoriadis S, Polyzoidou E, Milonas I, Karussis D. Neuroinflammation in multiple sclerosis: evidence for autoimmune dysregulation, not simple autoimmune reaction. Clin Neurol Neurosurg. 2006;108:241-244.
4. Gonzalez-Scarano F, Baltuch G. Microglia as mediators of inflammatory and degenerative diseases. Annu Rev Neurosci. 1999;22:219-240. (Pubitemid 29144887)
5. Minghetti L, Levi G. Microglia as effector cells in brain damage and repair: focus on prostanoids and nitric oxide. Prog Neurobiol. 1998;54:99-125. (Pubitemid 28049822)
6. Kreutzberg GW. Microglia: a sensor for pathological events in the cns. Trends Neurosci. 1996;19:312-318. (Pubitemid 26349059)
7. Rock RB, Gekker G, Hu S, Sheng WS, Cheeran M, Lokensgard JR, et al. Role of microglia in central nervous system infections. Clin Microbiol Rev. 2004;17:942-964. (Pubitemid 39372525)
8. Liu B, Hong JS. Role of microglia in inflammation-mediated neurodegenerative diseases: mechanisms and strategies for therapeutic intervention. J Pharmacol Exp Ther. 2003;304:1-7. (Pubitemid 36008905)
9. Levesque S, Wilson B, Gregoria V, Thorpe LB, Dallas S, Polikov VS, et al. Reactive microgliosis: extracellular micro-calpain and microglia-mediated dopaminergic neurotoxicity. Brain. 2010;133: 808-821.
10. Giuffrida A, McMahon LR. In vivo pharmacology of endo-cannabinoids and their metabolic inhibitors: therapeutic implications in parkinson's disease and abuse liability. Prostaglandins Other Lipid Mediat. 2010;91:90-103.
11. Engeli S, Jordan J. The endocannabinoid system: body weight and metabolic regulation. Clin Cornerstone. 2006;8 Suppl 4: S24-S35.
12. Walter L, Stella N. Cannabinoids and neuroinflammation. Br J Pharmacol. 2004;141:775-785. (Pubitemid 38446178)
13. Svizenska I, Dubovy P, Sulcova A. Cannabinoid receptors 1 and 2 (cb1 and cb2), their distribution, ligands and functional involvement in nervous system structures-a short review. Pharmacol Biochem Behav. 2008;90:501-511.
14. Mallet PE, Beninger RJ. The cannabinoid cb1 receptor antagonist sr141716a attenuates the memory impairment produced by delta9-tetrahydrocannabinol or anandamide. Psychopharmacology (Berl). 1998;140:11-19. (Pubitemid 28524302)
15. Cao X, Liang L, Hadcock JR, Iredale PA, Griffith DA, Menniti FS, et al. Blockade of cannabinoid type 1 receptors augments the antiparkinsonian action of levodopa without affecting dyskinesias in 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine-treated rhesus monkeys. J Pharmacol Exp Ther. 2007;323:318-326. (Pubitemid 47443281)
16. Kelsey JE, Harris O, Cassin J. The cb(1) antagonist rimonabant is adjunctively therapeutic as well as monotherapeutic in an animal model of parkinson's disease. Behav Brain Res. 2009;203:304-307.
17. Gonzalez S, Scorticati C, Garcia-Arencibia M, de Miguel R, Ramos JA, Fernandez-Ruiz J. Effects of rimonabant, a selective cannabinoid cb1 receptor antagonist, in a rat model of parkinson's disease. Brain Res. 2006;1073-1074:209-219.
18. Pertwee RG. The therapeutic potential of drugs that target cannabinoid receptors or modulate the tissue levels or actions of endocannabinoids. AAPS J. 2005;7:E625-E654.
19. Nakamura Y, Si QS, Kataoka K. Lipopolysaccharide-induced microglial activation in culture: temporal profiles of morphological change and release of cytokines and nitric oxide. Neurosci Res. 1999;35:95-100. (Pubitemid 29518400)
20. Kim BW, Koppula S, Kim IS, Lim HW, Hong SM, Han SD, et al. Anti-neuroinflammatory activity of kamebakaurin from isodon japonicus via inhibition of c-jun nh(2)-terminal kinase and p38 mitogen-activated protein kinase pathway in activated microglial cells. J Pharmacol Sci. 2011;116:296-308.
21. Pan XD, Chen XC, Zhu YG, Zhang J, Huang TW, Chen LM, et al. Neuroprotective role of tripchlorolide on inflammatory neurotoxicity induced by lipopolysaccharide-activated microglia. Biochem Pharmacol. 2008;76:362-372.
22. Jeon NR, Koppula S, Kim BW, Park SH, Lee HW, Choi DK. Mmhd [(s, e)-2-methyl-1-(2-methylthiazol-4-yl) hexa-1, 5-dien-ol], a novel synthetic compound derived from epothilone, suppresses nuclear factor-kappab-mediated cytokine expression in lipo polysaccharide-stimulated bv-2 microglia. J Pharmacol Sci. 2010;112:158-166.
23. Bocchini V, Mazzolla R, Barluzzi R, Blasi E, Sick P, Kettenmann H. An immortalized cell line expresses properties of activated microglial cells. J Neurosci Res. 1992;31:616-621.
24. Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR. Analysis of nitrate, nitrite, and [15n]nitrate in biological fluids. Anal Biochem. 1982;126:131-138. (Pubitemid 13203451)
25. An H, Kim IS, Koppula S, Kim BW, Park PJ, Lim BO, et al. Protective effects of gastrodia elata blume on mpp+-induced cytotoxicity in human dopaminergic sh-sy5y cells. J Ethno pharmacol. 2010;130:290-298.
26. Ko HM, Koppula S, Kim BW, Kim IS, Hwang BY, Suk K, et al. Inflexin attenuates proinflammatory responses and nuclear factor-kappab activation in lps-treated microglia. Eur J Pharmacol. 2010;633:98-106.
27. Lan R, Liu Q, Fan P, Lin S, Fernando SR, McCallion D, et al. Structure-activity relationships of pyrazole derivatives as cannabinoid receptor antagonists. J Med Chem. 1999;42:769-776. (Pubitemid 29110792)
28. Meng XL, Yang JY, Chen GL, Zhang LJ, Wang LH, Li J, et al. Rv09, a novel resveratrol analogue, inhibits no and tnf-alpha production by lps-activated microglia. Int Immunopharmacol. 2008;8:1074-1082.
29. Walter S, Letiembre M, Liu Y, Heine H, Penke B, Hao W, et al. Role of the toll-like receptor 4 in neuroinflammation in alzheimer's disease. Cell Physiol Biochem. 2007;20:947-956. (Pubitemid 350059737)
30. Kim EJ, Kwon KJ, Park JY, Lee SH, Moon CH, Baik EJ. Effects of peroxisome proliferator-activated receptor agonists on lps-induced neuronal death in mixed cortical neurons: associated with inos and cox-2. Brain Res. 2002;941:1-10. (Pubitemid 34603279)
31. Levi G, Minghetti L, Aloisi F. Regulation of prostanoid synthesis in microglial cells and effects of prostaglandin e2 on microglial functions. Biochimie. 1998;80:899-904.
32. Pinteaux E, Rothwell NJ, Boutin H. Neuroprotective actions of endogenous interleukin-1 receptor antagonist (il-1ra) are mediated by glia. Glia. 2006;53:551-556.
33. Taylor DL, Jones F, Kubota ES, Pocock JM. Stimulation of microglial metabotropic glutamate receptor mglu2 triggers tumor necrosis factor alpha-induced neurotoxicity in concert with microglial-derived fas ligand. J Neurosci. 2005;25:2952-2964. (Pubitemid 40389253)
34. Wen W, Sanelli T, Ge W, Strong W, Strong MJ. Activated microglial supernatant induced motor neuron cytotoxicity is associated with upregulation of the tnfr1 receptor. Neurosci Res. 2006;55:87-95.
35. Minogue AM, Barrett JP, Lynch MA. Lps-induced release of il-6 from glia modulates production of il-1beta in a jak2-dependent manner. J Neuroinflammation. 2012;9:126.
36. Bonizzi G, Karin M. The two nf-kappab activation pathways and their role in innate and adaptive immunity. Trends Immunol. 2004;25:280-288. (Pubitemid 38610351)
37. Carmody RJ, Chen YH. Nuclear factor-kappab: activation and regulation during toll-like receptor signaling. Cell Mol Immunol. 2007;4:31-41.
38. Da Silva J, Pierrat B, Mary JL, Lesslauer W. Blockade of p38 mitogen-activated protein kinase pathway inhibits inducible nitric-oxide synthase expression in mouse astrocytes. J Biol Chem. 1997;272:28373-28380. (Pubitemid 27517783)
39. Van Eldik LJ, Thompson WL, Ralay Ranaivo H, Behanna HA, Martin Watterson D. Glia proinflammatory cytokine upregula-tion as a therapeutic target for neurodegenerative diseases: function-based and target-based discovery approaches. Int Rev Neurobiol. 2007;82:277-296.
40. Ekdahl CT, Kokaia Z, Lindvall O. Brain inflammation and adult neurogenesis: the dual role of microglia. Neuroscience. 2009; 158:1021-1029.
41. Perry VH, Cunningham C, Holmes C. Systemic infections and inflammation affect chronic neurodegeneration. Nat Rev Immunol. 2007;7:161-167. (Pubitemid 46174862)
42. Nakajima K, Kohsaka S. Microglia: activation and their significance in the central nervous system. J Biochem. 2001;130: 169-175. (Pubitemid 32785862)
43. Klegeris A, McGeer EG, McGeer PL. Therapeutic approaches to inflammation in neurodegenerative disease. Curr Opin Neurol. 2007;20:351-357. (Pubitemid 46743120)
44. Svensson C, Fernaeus SZ, Part K, Reis K, Land T. Lps-induced inos expression in bv-2 cells is suppressed by an oxidative mechanism acting on the jnk pathway-a potential role for neuroprotection. Brain Res. 2010;1322:1-7.
45. Block ML, Hong JS. Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism. Prog Neurobiol. 2005;76:77-98. (Pubitemid 41242883)
46. Stella N. Endocannabinoid signaling in microglial cells. Neuro-pharmacology. 2009;56 Suppl 1:244-253.
47. Klein TW. Cannabinoid-based drugs as anti-inflammatory therapeutics. Nat Rev Immunol. 2005;5:400-411. (Pubitemid 40685989)
48. Little JP, Villanueva EB, Klegeris A. Therapeutic potential of cannabinoids in the treatment of neuroinflammation associated with parkinson's disease. Mini Rev Med Chem. 2011;11:582-590.
49. Kyrou I, Valsamakis G, Tsigos C. The endocannabinoid system as a target for the treatment of visceral obesity and metabolic syndrome. Ann N Y Acad Sci. 2006;1083:270-305. (Pubitemid 44955478)
50. Turu G, Hunyady L. Signal transduction of the cb1 cannabinoid receptor. J Mol Endocrinol. 2010;44:75-85.
51. Di Marzo V. Cb(1) receptor antagonism: Biological basis for metabolic effects. Drug Discov Today. 2008;13:1026-1041.
52. Sagredo O, Garcia-Arencibia M, de Lago E, Finetti S, Decio A, Fernandez-Ruiz J. Cannabinoids and neuroprotection in basal ganglia disorders. Mol Neurobiol. 2007;36:82-91. (Pubitemid 351360353)
53. Costa B, Trovato AE, Colleoni M, Giagnoni G, Zarini E, Croci T. Effect of the cannabinoid cb1 receptor antagonist, sr141716, on nociceptive response and nerve demyelination in rodents with chronic constriction injury of the sciatic nerve. Pain. 2005;116: 52-61. (Pubitemid 40828500)
54. Mnich SJ, Hiebsch RR, Huff RM, Muthian S. Anti-inflammatory properties of cb1-receptor antagonist involves beta2 adrenocep-tors. J Pharmacol Exp Ther. 2010;333:445-453.
55. Wang Q, Perrard XD, Perrard JL, Mansoori A, Smith CW, Ballantyne CM, et al. Effect of the cannabinoid receptor-1 antagonist rimonabant on inflammation in mice with diet-induced obesity. Obesity (Silver Spring). 2011;19:505-513.
56. Brown GC, Cooper CE. Nanomolar concentrations of nitric oxide reversibly inhibit synaptosomal respiration by competing with oxygen at cytochrome oxidase. FEBS Lett. 1994;356:295-298. (Pubitemid 24376992)
57. McGeer PL, Kawamata T, Walker DG, Akiyama H, Tooyama I, McGeer EG. Microglia in degenerative neurological disease. Glia. 1993;7:84-92.
58. Lau LM, Wolter JK, Lau JT, Cheng LS, Smith KM, Hansford LM, et al. Cyclooxygenase inhibitors differentially modulate p73 isoforms in neuroblastoma. Oncogene. 2009;28:2024-2033.
59. Minghetti L, Polazzi E, Nicolini A, Greco A, Levi G. Possible role of microglial prostanoids and free radicals in neuroprotec-tion and neurodegeneration. Adv Exp Med Biol. 1999;468: 109-119. (Pubitemid 32197925)
60. Teismann P, Vila M, Choi DK, Tieu K, Wu DC, Jackson-Lewis V, et al. Cox-2 and neurodegeneration in parkinson's disease. Ann N Y Acad Sci. 2003;991:272-277. (Pubitemid 36793820)
61. Wyss-Coray T, Mucke L. Inflammation in neurodegenerative disease-a double-edged sword. Neuron. 2002;35:419-432. (Pubitemid 34879943)
62. Kim SH, Smith CJ, Van Eldik LJ. Importance of mapk pathways for microglial pro-inflammatory cytokine il-1 beta production. Neurobiol Aging. 2004;25:431-439. (Pubitemid 38317340)
63. Ock J, Kim S, Yi KY, Kim NJ, Han HS, Cho JY, et al. A novel anti-neuroinflammatory pyridylimidazole compound kr-31360. Biochem Pharmacol. 2010;79:596-609.
64. Rahman A, Fazal F. Blocking nf-kappab: an inflammatory issue. Proc Am Thorac Soc. 2011;8:497-503.
65. Lim JY, Won TJ, Hwang BY, Kim HR, Hwang KW, Sul D, et al. The new diterpene isodojaponin d inhibited lps-induced microglial activation through nf-kappab and mapk signaling pathways. Eur J Pharmacol. 2010;642:10-18.
66. Tak PP, Firestein GS. Nf-kappab: a key role in inflammatory diseases. J Clin Invest. 2001;107:7-11. (Pubitemid 32047405)
67. Hwang J, Hwang H, Lee HW, Suk K. Microglia signaling as a target of donepezil. Neuropharmacology. 2010;58:1122-1129.
68. Krakauer T. Molecular therapeutic targets in inflammation: cyclooxygenase and nf-kappab. Curr Drug Targets Inflamm Allergy. 2004;3:317-324. (Pubitemid 39206661)
69. Lawrence T, Gilroy DW, Colville-Nash PR, Willoughby DA. Possible new role for nf-kappab in the resolution of inflammation. Nat Med. 2001;7:1291-1297. (Pubitemid 34007932)
70. Nomura Y. Nf-kappab activation and ikappab alpha dynamism involved in inos and chemokine induction in astroglial cells. Life Sci. 2001;68:1695-1701. (Pubitemid 32245618)
71. Liu HT, Du YG, He JL, Chen WJ, Li WM, Yang Z, et al. Tetra-methylpyrazine inhibits production of nitric oxide and inducible nitric oxide synthase in lipopolysaccharide-induced n9 microglial cells through blockade of mapk and pi3k/akt signaling pathways, and suppression of intracellular reactive oxygen species. J Ethno-pharmacol. 2010;129:335-343.
72. Kim EK, Choi EJ. Pathological roles of mapk signaling pathways in human diseases. Biochim Biophys Acta. 2010;1802:396-405.
73. Kaminska B, Gozdz A, Zawadzka M, Ellert-Miklaszewska A, Lipko M. Mapk signal transduction underlying brain inflammation and gliosis as therapeutic target. Anat Rec (Hoboken). 2009;292:1902-1913.
74. Harper SJ, Wilkie N. Mapks: new targets for neurodegeneration. Expert Opin Ther Targets. 2003;7:187-200. (Pubitemid 36512020)
75. Saccani S, Pantano S, Natoli G. P38-dependent marking of inflammatory genes for increased nf-kappa b recruitment. Nat Immunol. 2002;3:69-75. (Pubitemid 34065620)
76. Yasuda S, Sugiura H, Tanaka H, Takigami S, Yamagata K. P38 map kinase inhibitors as potential therapeutic drugs for neural diseases. Cent Nerv Syst Agents Med Chem. 2011;11:45-59.
77. Gomez-Nicola D, Valle-Argos B, Nieto-Sampedro M. Blockade of il-15 activity inhibits microglial activation through the nfkappab, p38, and erk1/2 pathways, reducing cytokine and chemokine release. Glia. 2010;58:264-276.
78. Munoz L, Ralay Ranaivo H, Roy SM, Hu W, Craft JM, McNamara LK, et al. A novel p38 alpha mapk inhibitor suppresses brain proinflammatory cytokine up-regulation and attenuates synaptic dysfunction and behavioral deficits in an alzheimer's disease mouse model. J Neuroinflammation. 2007; 4:21.