Anti-inflammatory efficacy of dexamethasone and Nrf2 activators in the CNS using brain slices as a model of acute injury

Journal of Neuroimmune Pharmacology

Volumn 7, Issue 1, 2012, Pages 266-278

  Graber, David J ^a   Hickey, William F ^a   Stommel, Elijah W ^a   Harris, Brent T ^a,b  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b GEORGETOWN UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cerebral cortex; Dexamethasone; Explant; Microglia; Nrf2 activation; Triterpenoid

Indexed keywords

DEXAMETHASONE; FUMARIC ACID DIMETHYL ESTER; INTERLEUKIN 1BETA; LUTEOLIN; MESSENGER RNA; QUERCETIN; TRANSCRIPTION FACTOR NRF2; TRITERPENOID; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BRAIN CORTEX; BRAIN INJURY; CELL CULTURE; CONTROLLED STUDY; DRUG EFFICACY; MICROGLIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; ANTI-INFLAMMATORY AGENTS; BRAIN; BRAIN INJURIES; DEXAMETHASONE; DISEASE MODELS, ANIMAL; FEMALE; INFLAMMATION; MICE; MICROGLIA; NF-E2-RELATED FACTOR 2; NITRIC OXIDE; ORGAN CULTURE TECHNIQUES; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRITERPENES;

EID: 84860721670     PISSN: 15571890     EISSN: 15571904     Source Type: Journal    
DOI: 10.1007/s11481-011-9338-8     Document Type: Article

References (59)

1. Babcock AA, Toft-Hansen H, Owens T (2008) Signaling through MyD88 regulates leukocyte recruitment after brain injury. J Immunol 181:6481-6490
2. Bartholdi D, Schwab ME (1997) Expression of pro-inflammatory cytokine and chemokine mRNA upon experimental spinal cord injury in mouse: an in situ hybridization study. Eur J Neurosci 9:1422-1438 (Pubitemid 27303243)
3. Bertorelli R, Adami M, Di Santo E, Ghezzi P (1998) MK 801 and dexamethasone reduce both tumor necrosis factor levels and infarct volume after focal cerebral ischemia in the rat brain. Neurosci Lett 246:41-44 (Pubitemid 28218361)
4. Calkins MJ, Johnson DA, Townsend JA, Vargas MR, Dowell JA, Williamson TP, Kraft AD, Lee JM, Li J, Johnson JA (2009) The Nrf2/ARE pathway as a potential therapeutic target in neurodegenerative disease. Antioxid Redox Sign 11:497-508
5. Castano A, Herrera AJ, Cano J, Machado A (2002) The degenerative effect of a single intranigral injection of LPS on the dopaminergic system is prevented by dexamethasone, and not mimicked by rh- TNF-alpha, IL-1beta and IFN-gamma. J Neurochem 81:150-157 (Pubitemid 34808862)
6. Chang RCC, Chiu K, Ho YS, So KF (2009) Modulation of neuroimmune responses on glia in the central nervous system: implication in therapeutic intervention against neuroinflammation. Cell Mol Immunol 5:317-326
7. Chen JC, Ho FM (2005) Inhibition of iNOS gene expression by quercetin is mediated by the inhibition of I [kappa] B kinase, nuclear factor-kappa B and STAT1, and depends on heme oxygenase-1 induction in mouse BV-2 microglia. Eur J Pharmacol 521:9-20
8. Chen XL, Kunsch C (2004) Induction of cytoprotective genes through Nrf2/antioxidant response element pathway: a new therapeutic approach for the treatment of inflammatory diseases. Curr Pharm Des 10:879-891 (Pubitemid 38380066)
9. Cho S, Wood A, Bowlby MR (2007) Brain slices as models for neurodegenerative disease and screening platforms to identify novel therapeutics. Curr Neuropharmacol 5:19-33 (Pubitemid 46488264)
10. Dallas S, Zhu X, Baruchel S, Schlichter L, Bendayan R (2003) Functional expression of the multidrug resistance protein 1 in microglia. J Pharmacol Exp Ther 307:282-290 (Pubitemid 37151919)
11. Dallas S, Schlichter L, Bendayan R (2004) Multidrug resistance protein (MRP) 4-and MRP 5-mediated efflux of 9-(2-phosphonylmethoxyethyl) adenine by microglia. J Pharmacol Exp Ther 309:1221-1221
12. Dinkova-Kostova AT, Holtzclaw WD, Cole RN, Itoh K, Wakabayashi N, Katoh Y, Yamamoto M, Talalay P (2002) Direct evidence that sulfhydryl groups of Keap1 are the sensors regulating induction of phase 2 enzymes that protect against carcinogens and oxidants. Proc Natl Acad Sci U S A 99:11908-11913 (Pubitemid 34994497)
13. Dumont M, Wille E, Calingasan NY, Tampellini D, Williams C, Gouras GK, Liby K, Sporn M, Beal MF, Lin MT (2009) Triterpenoid CDDO-methylamide improves memory and decreases amyloid plaques in a transgenic mouse model of Alzheimer's disease. J Neurochem 109:502-512
14. Esen N, Kielian T (2006) Central role for MyD88 in the responses of microglia to pathogen-associated molecular patterns. J Immunol 176:6802-6811 (Pubitemid 43787863)
15. Ford AL, Goodsall AL, Hickey WF, Sedgwick JD (1995) Normal adult ramified microglia separated from other central nervous system macrophages by flow cytometric sorting. Phenotypic differences defined and direct ex vivo antigen presentation to myelin basic protein-reactive CD4 T cells compared. J Immunol 154:4309-4321
16. Gekeler V, Ise W, Sanders KH, Ulrich WR, Beck J (1995) The leukotriene LTD4 receptor antagonist MK571 specifically modulates MRP associated multidrug resistance. Biochem Biophys Res Commun 208:345-352
17. Graber DJ, Park PJ, Hickey WF, Harris BT (2011) Synthetic triterpenoid CDDO derivatives modulate cytoprotective or immunological properties in astrocytes, neurons, and microglia. J Neuroimmune Pharmacol 6:107-120
18. Honda T, Honda Y, Favaloro FG, Gribble GW, Suh N, Place AE, Rendi MH, Sporn MB (2002) A novel dicyanotriterpenoid, 2-cyano-3, 12-dioxooleana-1, 9 (11)-dien-28-onitrile, active at picomolar concentrations for inhibition of nitric oxide production. Bioorg Med Chem Lett 12:1027-1030 (Pubitemid 34242794)
19. Huscher D, Thiele K, Gromnica-Ihle E, Hein G, Demary W, Dreher R, Zink A, Buttgereit F (2009) Dose-related patterns of glucocorticoidinduced side effects. Ann Rheum Dis 68:1119-1124
20. Huuskonen J, Suuronen T, Miettinen R, van Groen T, Salminen A (2005) A refined in vitro model to study inflammatory responses in organotypic membrane culture of postnatal rat hippocampal slices. J Neuroinflammation 2:25
21. Innamorato NG, Rojo AI, Garcia-Yague AJ, Yamamoto M, de Ceballos ML, Cuadrado A (2008) The transcription factor Nrf2 is a therapeutic target against brain inflammation. J Immunol 181:680-689
22. Itoh K, Wakabayashi N, Katoh Y, Ishii T, Igarashi K, Engel JD, Yamamoto M (1999) Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev 13:76-86 (Pubitemid 29045117)
23. Jin W, Zhu L, Guan Q, Chen G, Wang QF, Yin HX, Hang CH, Shi JX, Wang HD (2008) Influence of Nrf2 genotype on pulmonary NF- {kappa} B activity and inflammatory response after traumatic brain injury. Ann Clin Lab Sci 38:221-227
24. Jonat C, Rahmsdorf HJ, Park KK, Cato ACB, Gebel S, Ponta H, Herrlich P (1990) Antitumor promotion and anti-inflammation: down-modulation of AP-1 (Fos/Jun) activity by glucocorticoid hormone. Cell 62:1189-1204
25. Kassel O, Sancono A, Krätzschmar J, Kreft B, Stassen M, Cato ACB (2001) Glucocorticoids inhibit MAP kinase via increased expression and decreased degradation of MKP-1. EMBO J 20:7108-7116 (Pubitemid 34062302)
26. Kensler TW, Wakabayashi N, Biswal S (2007) Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol 47:89-116
27. Knerlich F, Schilling L, Görlach C, Wahl M, Ehrenreich H, Sirén AL (1999) Temporal profile of expression and cellular localization of inducible nitric oxide synthase, interleukin-1 [beta] and interleukin converting enzyme after cryogenic lesion of the rat parietal cortex. Mol Brain Res 68:73-87 (Pubitemid 29243996)
28. Kurkowska-Jastrzbska I, Litwin T, Joniec I, Ciesielska A, Przybykowski A, Czonkowski A, Czonkowska A (2004) Dexamethasone protects against dopaminergic neurons damage in a mouse model of Parkinson's disease. Int Immunopharmacol 4:1307-1318 (Pubitemid 39094405)
29. Lee G, Schlichter L, Bendayan M, Bendayan R (2001) Functional expression of P-glycoprotein in rat brain microglia. J Pharmacol Exp Ther 299:204-212 (Pubitemid 32905136)
30. Lee JM, Li J, Johnson DA, Stein TD, Kraft AD, Calkins MJ, Jakel RJ, Johnson JA (2005) Nrf2, a multi-organ protector? FASEB J 19:1061-1066 (Pubitemid 40946431)
31. Liby K, Hock T, Yore MM, Suh N, Place AE, Risingsong R, Williams CR, Royce DB, Honda T, Honda Y (2005) The synthetic triterpenoids, CDDO and CDDO-imidazolide, are potent inducers of heme oxygenase-1 and Nrf2/ARE signaling. Cancer Res 65:4789-4798 (Pubitemid 40740817)
32. Lin W, Wu RT, Wu T, Khor T, Wang H, Kong A (2008) Sulforaphane suppressed LPS-induced inflammation in mouse peritoneal macrophages through Nrf2 dependent pathway. Biochem Pharmacol 76:967-973
33. Liu Z, Bendayan R, Wu XY (2001) Triton-X-100-modified polymer and microspheres for reversal of multidrug resistance. J Pharm Pharmacol 53:779-787 (Pubitemid 32529720)
34. Lossi L, Alasia S, Salio C, Merighi A (2009) Cell death and proliferation in acute slices and organotypic cultures of mammalian CNS. Prog Neurobiol 88:221-245
35. Minami M, Kuraishi Y, Yamaguchi T, Nakai S, Hirai Y, Satoh M (1990) Convulsants induce interleukin-1 [beta] messenger RNA in rat brain. Biochem Biophys Res Commun 171:832-837 (Pubitemid 20289459)
36. Neymotin A, Calingasan NY, Wille E, Naseri N, Petri S, Damiano M, Liby KT, Risingsong R, Sporn M, Beal MF (2011) Neuroprotective effect of Nrf2/ARE activators, CDDO-ethylamide and CDDO-trifluoroethylamide in a mouse model of amyotrophic lateral sclerosis. Free Radic Biol Med 51:88-96
37. Ohtsuka T, Kubota A, Hirano T, Watanabe K, Yoshida H, Tsurufuji M, Iizuka Y, Konishi K, Tsurufuji S (1996) Glucocorticoid-mediated gene suppression of rat cytokine-induced neutrophil chemoattractant CINC/gro, a member of the interleukin-8 family, through impairment of NF-kappa B activation. J Biol Chem 271:1651-1669
38. Osburn WO, Yates MS, Dolan PD, Chen S, Liby KT, Sporn MB, Taguchi K, Yamamoto M, Kensler TW (2008) Genetic or pharmacologic amplification of nrf2 signaling inhibits acute inflammatory liver injury in mice. Toxicol Sci 104:218-227 (Pubitemid 351859044)
39. Pan JZ, Ni L, Sodhi A, Aguanno A, YoungW, Hart RP (2002) Cytokine activity contributes to induction of inflammatory cytokine mRNAs in spinal cord following contusion. J Neurosci Res 68:315-322 (Pubitemid 34462536)
40. Reddy NM, Suryanaraya V, Yates MS, Kleeberger SR, Hassoun PM, Yamamoto M, Liby KT, Sporn MB, Kensler TW, Reddy SP (2009) The triterpenoid CDDO-imidazolide confers potent protection against hyperoxic acute lung injury in mice. Am J Respir Crit Care Med 180:867-874
41. Reid G, Wielinga P, Zelcer N, De Haas M, Van Deemter L, Wijnholds J, Balzarini J, Borst P (2003) Characterization of the transport of nucleoside analog drugs by the human multidrug resistance proteins MRP4 and MRP5. Mol Pharmacol 63:1094-1103 (Pubitemid 36529928)
42. Rice T, Larsen J, Rivest S, Yong VW (2007) Characterization of the early neuroinflammation after spinal cord injury in mice. J Neuropathol Exp Neurol 66:184-195 (Pubitemid 46673274)
43. Rushworth SA, MacEwan DJ, O'ConnellMA (2008) Lipopolysaccharideinduced expression of NAD (P) H: quinone oxidoreductase 1 and heme oxygenase-1 protects against excessive inflammatory responses in human monocytes. J Immunol 181:6730-6737
44. Schäcke H, Döcke WD, Asadullah K (2002) Mechanisms involved in the side effects of glucocorticoids. Pharmacol Ther 96:23-43 (Pubitemid 35346616)
45. Sinz EH, Kochanek PM, Dixon CE, Clark RSB, Carcillo JA, Schiding JK, Chen M, Wisniewski SR, Carlos TM, Williams D (1999) Inducible nitric oxide synthase is an endogenous neuroprotectant after traumatic brain injury in rats and mice. J Clin Invest 104:647-668
46. Stack C, Ho D, Wille E, Calingasan NY, Williams C, Liby K, Sporn M, Dumont M, Beal MF (2010) Triterpenoids CDDO-ethyl amide and CDDO-trifluoroethyl amide improve the behavioral phenotype and brain pathology in a transgenic mouse model of Huntington's disease. Free Radic Biol Med 49:147-158
47. Stahn C, Löwenberg M, Hommes DW, Buttgereit F (2007) Molecular mechanisms of glucocorticoid action and selective glucocorticoid receptor agonists. Mol Cell Endocrinol 275:71-78 (Pubitemid 47259281)
48. Suh N, Wang Y, Honda T, Gribble GW, Dmitrovsky E, Hickey WF, Maue RA, Place AE, Porter DM, Spinella MJ, Williams CR, Wu G, Dannenberg AJ, Flanders KC, Letterio JJ, Mangelsdorf DJ, Nathan CF, Nguyen L, Porter WW, Ren RF, Roberts AB, Roche NS, Subbaramaiah K, Sporn MB (1999) A novel synthetic oleanane triterpenoid, 2-cyano-3, 12-dioxoolean-1, 9-dien-28-oic acid, with potent differentiating, antiproliferative, and anti-inflammatory activity. Cancer Res 59:336-341
49. Sussan TE, Rangasamy T, Blake DJ, Malhotra D, El-Haddad H, Bedja D, Yates MS, Kombairaju P, Yamamoto M, Liby KT (2009) Targeting Nrf2 with the triterpenoid CDDO-imidazolide attenuates cigarette smoke-induced emphysema and cardiac dysfunction in mice. Proc Natl Acad Sci U S A 106:250-255
50. Thimmulappa RK, Scollick C, Traore K, Yates M, Trush MA, Liby KT, Sporn MB, Yamamoto M, Kensler TW, Biswal S (2006) Nrf2 dependent protection from LPS induced inflammatory response and mortality by CDDO-imidazolide. Biochem Biophys Res Commun 351:883-889 (Pubitemid 44715868)
51. Tran TA, McCoy MK, Sporn MB, Tansey MG (2008) The synthetic triterpenoid CDDO-methyl ester modulates microglial activities, inhibits TNF production, and provides dopaminergic neuroprotection. J Neuroinflammation 5:14
52. Wang J, Fields J, Zhao C, Langer J, Thimmulappa RK, Kensler TW, Yamamoto M, Biswal S, Doré S (2007) Role of Nrf2 in protection against intracerebral hemorrhage injury in mice. Free Radic Biol Med 43:408-414 (Pubitemid 46977628)
53. Wilms H, Sievers J, Rickert U, Rostami-Yazdi M, Mrowietz U, Lucius R (2010) Dimethylfumarate inhibits microglial and astrocytic inflammation by suppressing the synthesis of nitric oxide, IL- 1β, TNF-α and IL-6 in an in-vitro model of brain inflammation. J Neuroinflammation 7:30
54. Wollmer MA, Lucius R,Wilms H, Held-Feindt J, Sievers J, Mentlein R (2001) ATP and adenosine induce ramification of microglia in vitro. J Neuroimmunol 115:19-27 (Pubitemid 32245649)
55. Xu W, Hellerbrand C, Köhler UA, Bugnon P, Kan YW, Werner S, Beyer TA (2008) The Nrf2 transcription factor protects from toxin-induced liver injury and fibrosis. Lab Investig 88:1068-1078
56. Yang L, Calingasan NY, Thomas B, Chaturvedi RK, Kiaei M, Wille EJ, Liby KT, Williams C, Royce D, Risingsong R, Musiek ES, Morrow JD, Sporn M, Beal MF (2009) Neuroprotective effects of the triterpenoid, CDDO methyl amide, a potent inducer of Nrf2- mediated transcription. PLoS One 4:e5757
57. Yates MS, Tauchi M, Katsuoka F, Flanders KC, Liby KT, Honda T, Gribble GW, Johnson DA, Johnson JA, Burton NC, Guilarte TR, Yamamoto M, Sporn MB, Kensler TW (2007) Pharmacodynamic characterization of chemopreventive triterpenoids as exceptionally potent inducers of Nrf2-regulated genes. Mol Cancer Ther 6:154-162 (Pubitemid 46206678)
58. Zhang Z, Zhang Z, Artelt M, Burnet M, Schluesener HJ (2007) Dexamethasone attenuates early expression of three molecules associated with microglia/macrophages activation following rat traumatic brain injury. Acta Neuropathol 113:675-682 (Pubitemid 46863903)
59. Zordan-Nudo T, Ling V, Liu Z, Georges E (1993) Effects of nonionic detergents on P-glycoprotein drug binding and reversal of multidrug resistance. Cancer Res 53:5994-6000 (Pubitemid 24006172)