Comparison of anti-inflammatory potential of four different dibenzocyclooctadiene lignans in microglia; action via activation of PKA and Nrf-2 signaling and inhibition of MAPK/STAT/NF-κB pathways

Molecular Nutrition and Food Research

Volumn 58, Issue 4, 2014, Pages 738-748

  Park, Sun Young ^a   Bae, Yoe Sik ^b   Ko, Min Jung ^a   Lee, Sang Joon ^a   Choi, Young Whan ^a  

^a Pusan National University   (South Korea)

^b Sungkyunkwan University   (South Korea)

Author keywords

Antineuroinflammation; Dibenzocyclooctadiene lignans; Microglia; Phase II detoxifying antioxidant enzymes; TLR 2 4 agonists

Indexed keywords

1,3 DIOXOLANE DERIVATIVE; AMYLOID BETA PROTEIN; ANTIOXIDANT; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLOOCTANE DERIVATIVE; DIBENZOCYCLOOCTADIENE LIGNAN; GOMISIN; GOMISIN A; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIGNAN; LIPOPOLYSACCHARIDE; NEUROPROTECTIVE AGENT; NFE2L2 PROTEIN, MOUSE; NONSTEROID ANTIINFLAMMATORY AGENT; POLYCYCLIC HYDROCARBON; REACTIVE OXYGEN METABOLITE; SCHIZANDRER A; SCHIZANDRIN B; STAT PROTEIN; TLR2 PROTEIN, MOUSE; TOLL LIKE RECEPTOR 2; TRANSCRIPTION FACTOR NRF2;

AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; COMPARATIVE STUDY; DRUG EFFECTS; INSTITUTE FOR CANCER RESEARCH MOUSE; METABOLISM; MICROGLIA; SIGNAL TRANSDUCTION;

AMYLOID BETA-PEPTIDES; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ANTIOXIDANTS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYCLOOCTANES; DIOXOLES; LIGNANS; LIPOPOLYSACCHARIDES; MAP KINASE SIGNALING SYSTEM; MICE, INBRED ICR; MICROGLIA; NEUROPROTECTIVE AGENTS; NF-E2-RELATED FACTOR 2; NF-KAPPA B; POLYCYCLIC COMPOUNDS; REACTIVE OXYGEN SPECIES; STAT TRANSCRIPTION FACTORS; TOLL-LIKE RECEPTOR 2;

EID: 84897057421     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201300445     Document Type: Article

References (37)

1. Wilms, H., Rosenstiel, P., Sievers, J., Deuschl, G. et al., Activation of microglia by human neuromelanin is NF-kappaB dependent and involves p38 mitogen-activated protein kinase: implications for Parkinson's disease. FASEB J. 2003, 17, 500-502.
2. Rodriguez-Pallares, J., Rey, P., Parga, J. A., Munoz, A. et al., Brain angiotensin enhances dopaminergic cell death via microglial activation and NADPH-derived ROS. Neurobiol. Dis. 2008, 31, 58-73.
3. Lorenzl, S., Albers, D. S., Relkin, N., Ngyuen, T. et al., Increased plasma levels of matrix metalloproteinase-9 in patients with Alzheimer's disease. Neurochem. Int. 2003, 43, 191-196.
4. Lotz, M., Ebert, S., Esselmann, H., Iliev, A. I. et al., Amyloid beta peptide 1-40 enhances the action of Toll-like receptor-2 and -4 agonists but antagonizes Toll-like receptor-9-induced inflammation in primary mouse microglial cell cultures. J. Neurochem. 2005, 94, 289-298.
5. Olson, J. K., Miller, S. D., Microglia initiate central nervous system innate and adaptive immune responses through multiple TLRs. J. Immunol. 2004, 173, 3916-3924.
6. Jack, C. S., Arbour, N., Manusow, J., Montgrain, V. et al., TLR signaling tailors innate immune responses in human microglia and astrocytes. J. Immunol. 2005, 175, 4320-4330.
7. Lee, S. J., Lee, S., Toll-like receptors and inflammation in the CNS. Curr. Drug Targets Inflamm. Allergy. 2002, 1, 181-191.
8. Dhawan, G., Combs, C. K., Inhibition of Src kinase activity attenuates amyloid associated microgliosis in a murine model of Alzheimer's disease. J. Neuroinflam. 2012, 9, 117-2094-9-117.
9. Jung, D. Y., Lee, H., Jung, B. Y., Ock, J. et al., TLR4, but not TLR2, signals autoregulatory apoptosis of cultured microglia: a critical role of IFN-beta as a decision maker. J. Immunol. 2005, 174, 6467-6476.
10. Ribes, S., Ebert, S., Regen, T., Agarwal, A. et al., Toll-like receptor stimulation enhances phagocytosis and intracellular killing of nonencapsulated and encapsulated Streptococcus pneumoniae by murine microglia. Infect. Immun. 2010, 78, 865-871.
11. Eikelenboom, P., Veerhuis, R., Familian, A., Hoozemans, J. J. et al., Neuroinflammation in plaque and vascular beta-amyloid disorders: clinical and therapeutic implications. Neurodegener. Dis. 2008, 5, 190-193.
12. Lastres-Becker, I., Ulusoy, A., Innamorato, N. G., Sahin, G. et al., alpha-Synuclein expression and Nrf2 deficiency cooperate to aggravate protein aggregation, neuronal death and inflammation in early-stage Parkinson's disease. Hum. Mol. Genet. 2012, 21, 3173-3192.
13. Kim, S. E., Lee, E. O., Yang, J. H., Kang, J. H. et al., 15-deoxy-delta(1)(2), (1)(4)-prostaglandin J(2) inhibits human immunodeficiency virus-1 tat-induced monocyte chemoattractant protein-1/CCL2 production by blocking the extracellular signal-regulated kinase-1/2 signaling pathway independently of peroxisome proliferator-activated receptor-gamma and heme oxygenase-1 in rat hippocampal slices. J. Neurosci. Res. 2012, 90, 1732-1742.
14. Innamorato, N. G., Lastres-Becker, I., Cuadrado, A., Role of microglial redox balance in modulation of neuroinflammation. Curr. Opin. Neurol. 2009, 22, 308-314.
15. Innamorato, N. G., Rojo, A. I., Garcia-Yague, A. J., Yamamoto, M. et al., The transcription factor Nrf2 is a therapeutic target against brain inflammation. J. Immunol. 2008, 181, 680-689.
16. Jang, S., Kelley, K. W., Johnson, R. W., Luteolin reduces IL-6 production in microglia by inhibiting JNK phosphorylation and activation of AP-1. Proc. Natl. Acad. Sci. U. S. A. 2008, 105, 7534-7539.
17. Jung, J. S., Kim, D. H., Kim, H. S., Ginsenoside Rh1 suppresses inducible nitric oxide synthase gene expression in IFN-gamma-stimulated microglia via modulation of JAK/STAT and ERK signaling pathways. Biochem. Biophys. Res. Commun. 2010, 397, 323-328.
18. Mu, H. X., Li, X. S., Fan, P., Yang, G. Y. et al., Dibenzocyclooctadiene lignans from the fruits of Schisandra rubriflora and their anti-HIV-1 activities. J. Asian Nat. Prod. Res. 2011, 13, 393-399.
19. Yang, J. H., Zhang, H. Y., Wen, J., Du, X. et al., Dibenzocyclooctadiene lignans with antineurodegenerative potential from Kadsura ananosma. J. Nat. Prod. 2011, 74, 1028-1035.
20. Choi, Y. W., Takamatsu, S., Khan, S. I., Srinivas, P. V. et al., Schisandrene, a dibenzocyclooctadiene lignan from Schisandra chinensis: structure-antioxidant activity relationships of dibenzocyclooctadiene lignans. J. Nat. Prod. 2006, 69, 356-359.
21. Waiwut, P., Shin, M. S., Inujima, A., Zhou, Y. et al., Gomisin N enhances TNF-alpha-induced apoptosis via inhibition of the NF-kappaB and EGFR survival pathways. Mol. Cell. Biochem. 2011, 350, 169-175.
22. Kim, S. R., Lee, M. K., Koo, K. A., Kim, S. H. et al., Dibenzocyclooctadiene lignans from Schisandra chinensis protect primary cultures of rat cortical cells from glutamate-induced toxicity. J. Neurosci. Res. 2004, 76, 397-405.
23. Giulian, D., Baker, T. J., Characterization of ameboid microglia isolated from developing mammalian brain. J. Neurosci. 1986, 6, 2163-2178.
24. Im, J. Y., Kim, D., Lee, K. W., Kim, J. B. et al., COX-2 regulates the insulin-like growth factor I-induced potentiation of Zn(2+)-toxicity in primary cortical culture. Mol. Pharmacol. 2004, 66, 368-376.
25. Johnson, K. D., Bresnick, E. H., Dissecting long-range transcriptional mechanisms by chromatin immunoprecipitation. Methods 2002, 26, 27-36.
26. Liu, C. L., Chiu, Y. T., Hu, M. L., Fucoxanthin enhances HO-1 and NQO1 expression in murine hepatic BNL CL.2 cells through activation of the Nrf2/ARE system partially by its pro-oxidant activity. J. Agric. Food Chem. 2011, 59, 11344-11351.
27. Lin, Y. C., Uang, H. W., Lin, R. J., Chen, I. J. et al., Neuroprotective effects of glyceryl nonivamide against microglia-like cells and 6-hydroxydopamine-induced neurotoxicity in SH-SY5Y human dopaminergic neuroblastoma cells. J. Pharmacol. Exp. Ther. 2007, 323, 877-887.
28. Min, H. Y., Park, E. J., Hong, J. Y., Kang, Y. J. et al., Antiproliferative effects of dibenzocyclooctadiene lignans isolated from Schisandra chinensis in human cancer cells. Bioorg. Med. Chem. Lett. 2008, 18, 523-526.
29. Choi, Y. W., Kim, K., Jo, J. Y., Kim, H. L. et al., Wuweizisu C from Schisandra chinensis decreases membrane potential in C6 glioma cells. Acta Pharmacol. Sin. 2008, 29, 1006-1012.
30. Lee, S. K., Kim, S. D., Lee, H. Y., Baek, S. H. et al., alpha-Iso-cubebene, a natural compound isolated from Schisandra chinensis fruit, has therapeutic benefit against polymicrobial sepsis. Biochem. Biophys. Res. Commun. 2012, 426, 226-231.
31. Dai, J. N., Zong, Y., Zhong, L. M., Li, Y. M. et al., Gastrodin inhibits expression of inducible NO synthase, cyclooxygenase-2 and proinflammatory cytokines in cultured LPS-stimulated microglia via MAPK pathways. PLoS One 2011, 6, e21891.
32. Park, S. H., Kang, J. S., Yoon, Y. D., Lee, K. et al., Glabridin inhibits lipopolysaccharide-induced activation of a microglial cell line, BV-2, by blocking NF-kappaB and AP-1. Phytother. Res. 2010, 24(Suppl. 1), S29-S34.
33. Kacimi, R., Giffard, R. G., Yenari, M. A., Endotoxin-activated microglia injure brain derived endothelial cells via NF-kappaB, JAK-STAT and JNK stress kinase pathways. J. Inflamm. (Lond). 2011, 8, 7-9255-8-7.
34. Yan, W., Wang, H. D., Hu, Z. G., Wang, Q. F. et al., Activation of Nrf2-ARE pathway in brain after traumatic brain injury. Neurosci. Lett. 2008, 431, 150-154.
35. Lastres-Becker, I., Ulusoy, A., Innamorato, N. G., Sahin, G. et al., alpha-Synuclein expression and Nrf2 deficiency cooperate to aggravate protein aggregation, neuronal death and inflammation in early-stage Parkinson's disease. Hum. Mol. Genet. 2012, 21, 3173-3192.
36. Ziady, A. G., Sokolow, A., Shank, S., Corey, D. et al., Interaction with CREB binding protein modulates the activities of Nrf2 and NF-kappaB in cystic fibrosis airway epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 2012, 302, L1221-L1231.
37. Smith, K. T., Nicholls, R. D., Reines, D., The gene encoding the fragile X RNA-binding protein is controlled by nuclear respiratory factor 2 and the CREB family of transcription factors. Nucleic Acids Res. 2006, 34, 1205-1215.