Therapeutic targeting of Krüppel-like factor 4 abrogates microglial activation

Journal of Neuroinflammation

Volumn 9, Issue , 2012, Pages

  Kaushik, Deepak K ^a   Mukhopadhyay, Rupanjan ^a   Kumawat, Kanhaiya L ^a   Gupta, Malvika ^a   Basu, Anirban ^a  

^a NATIONAL BRAIN RESEARCH CENTRE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

HONOKIOL; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; KRUPPEL LIKE FACTOR 4; LIPOPOLYSACCHARIDE; CYCLOOXYGENASE 2; CYTOKINE; INDUCIBLE NITRIC OXIDE SYNTHASE; KRUPPEL LIKE FACTOR; POLYSACCHARIDE; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL STIMULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; ENCEPHALITIS; ENZYME SYNTHESIS; IN VITRO STUDY; IN VIVO STUDY; MICROGLIA; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN TARGETING; UPREGULATION; ANIMAL; BAGG ALBINO MOUSE; CELL LINE; CHEMICALLY INDUCED DISORDER; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECT; INFLAMMATION; METABOLISM;

ANIMALS; CELL LINE, TRANSFORMED; CYCLOOXYGENASE 2; CYTOKINES; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; INFLAMMATION; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; MICE, INBRED BALB C; MICROGLIA; NF-KAPPA B; NITRIC OXIDE SYNTHASE TYPE II; POLYSACCHARIDES; REACTIVE OXYGEN SPECIES;

EID: 84858328096     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-9-57     Document Type: Article

References (52)

1. Carson MJ, Thrash JC, Lo D. Analysis of microglial gene expression: identifying targets for CNS neurodegenerative and autoimmune disease. Am J Pharmacogenomics 2004, 4:321-330. 10.2165/00129785-200404050-00005, 15462610.
2. Kreutzberg GW. Microglia: a sensor for pathological events in the CNS. Trends Neurosci 1996, 19:312-318. 10.1016/0166-2236(96)10049-7, 8843599.
3. Lund S, Christensen KV, Hedtjarn M, Mortensen AL, Hagberg H, Falsig J, Hasseldam H, Schrattenholz A, Porzgen P, Leist M. The dynamics of the LPS triggered inflammatory response of murine microglia under different culture and in vivo conditions. J Neuroimmunol 2006, 180:71-87. 10.1016/j.jneuroim.2006.07.007, 16996144.
4. Qin L, Wu X, Block ML, Liu Y, Breese GR, Hong JS, Knapp DJ, Crews FT. Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia 2007, 55:453-462. 10.1002/glia.20467, 2871685, 17203472.
5. Rhee SH, Hwang D. Murine TOLL-like receptor 4 confers lipopolysaccharide responsiveness as determined by activation of NF kappa B and expression of the inducible cyclooxygenase. J Biol Chem 2000, 275:34035-34040.
6. Surh YJ, Chun KS, Cha HH, Han SS, Keum YS, Park KK, Lee SS. Molecular mechanisms underlying chemopreventive activities of anti-inflammatory phytochemicals: down-regulation of COX-2 and iNOS through suppression of NF-kappa B activation. Mutat Res 2001, 480-481:243-268.
7. Brown GC, Neher JJ. Inflammatory neurodegeneration and mechanisms of microglial killing of neurons. Mol Neurobiol 2010, 41:242-247. 10.1007/s12035-010-8105-9, 20195798.
8. Perry VH, Nicoll JA, Holmes C. Microglia in neurodegenerative disease. Nat Rev Neurol 2010, 6:193-201. 10.1038/nrneurol.2010.17, 20234358.
9. Carson MJ. Microglia as liaisons between the immune and central nervous systems: functional implications for multiple sclerosis. Glia 2002, 40:218-231. 10.1002/glia.10145, 2693029, 12379909.
10. Kim YS, Joh TH. Microglia, major player in the brain inflammation: their roles in the pathogenesis of Parkinson's disease. Exp Mol Med 2006, 38:333-347.
11. Hamik A, Lin Z, Kumar A, Balcells M, Sinha S, Katz J, Feinberg MW, Gerzsten RE, Edelman ER, Jain MK. Kruppel-like factor 4 regulates endothelial inflammation. J Biol Chem 2007, 282:13769-13779. 10.1074/jbc.M700078200, 17339326.
12. Feinberg MW, Cao Z, Wara AK, Lebedeva MA, Senbanerjee S, Jain MK. Kruppel-like factor 4 is a mediator of proinflammatory signaling in macrophages. J Biol Chem 2005, 280:38247-38258. 10.1074/jbc.M509378200, 16169848.
13. Yoon HS, Chen X, Yang VW. Kruppel-like factor 4 mediates p53-dependent G1/S cell cycle arrest in response to DNA damage. J Biol Chem 2003, 278:2101-2105. 10.1074/jbc.M211027200, 2229830, 12427745.
14. Liu J, Liu Y, Zhang H, Chen G, Wang K, Xiao X. KLF4 promotes the expression, translocation, and release of HMGB1 in RAW264.7 macrophages in response to LPS. Shock 2008, 30:260-266.
15. Shen B, Smith RS, Hsu YT, Chao L, Chao J. Kruppel-like factor 4 is a novel mediator of Kallistatin in inhibiting endothelial inflammation via increased endothelial nitric-oxide synthase expression. J Biol Chem 2009, 284:35471-35478. 10.1074/jbc.M109.046813, 2790976, 19858207.
16. Alder JK, Georgantas RW, Hildreth RL, Kaplan IM, Morisot S, Yu X, McDevitt M, Civin CI. Kruppel-like factor 4 is essential for inflammatory monocyte differentiation in vivo. J Immunol 2008, 180:5645-5652. 3074963, 18390749.
17. Segre JA, Bauer C, Fuchs E. Klf4 is a transcription factor required for establishing the barrier function of the skin. Nat Genet 1999, 22:356-360. 10.1038/11926, 10431239.
18. Katz JP, Perreault N, Goldstein BG, Lee CS, Labosky PA, Yang VW, Kaestner KH. The zinc-finger transcription factor Klf4 is required for terminal differentiation of goblet cells in the colon. Development 2002, 129:2619-2628. 2225535, 12015290.
19. Kaushik DK, Gupta M, Das S, Basu A. Kruppel-like factor 4, a novel transcription factor regulates microglial activation and subsequent neuroinflammation. J Neuroinflammation 2010, 7:68. 10.1186/1742-2094-7-68, 2965135, 20946687.
20. Shen CC, Ni CL, Shen YC, Huang YL, Kuo CH, Wu TS, Chen CC. Phenolic constituents from the stem bark of Magnolia officinalis. J Nat Prod 2009, 72:168-171. 10.1021/np800494e, 19086868.
21. Lin YR, Chen HH, Ko CH, Chan MH. Neuroprotective activity of honokiol and magnolol in cerebellar granule cell damage. Eur J Pharmacol 2006, 537:64-69. 10.1016/j.ejphar.2006.03.035, 16631734.
22. Wang X, Duan X, Yang G, Zhang X, Deng L, Zheng H, Deng C, Wen J, Wang N, Peng C, Zhao X, Wei Y, Chen L. Honokiol crosses BBB and BCSFB, and inhibits brain tumor growth in rat 9 L intracerebral gliosarcoma model and human U251 xenograft glioma model. PLoS One 2011, 6:e18490. 10.1371/journal.pone.0018490, 3084695, 21559510.
23. Fried LE, Arbiser JL. Honokiol, a multifunctional antiangiogenic and antitumor agent. Antioxid Redox Signal 2009, 11:1139-1148. 10.1089/ars.2009.2440, 2842137, 19203212.
24. Lin YR, Chen HH, Ko CH, Chan MH. Effects of honokiol and magnolol on acute and inflammatory pain models in mice. Life Sci 2007, 81:1071-1078. 10.1016/j.lfs.2007.08.014, 17826802.
25. Lee SY, Cho JY. Inhibitory effects of honokiol on LPS and PMA-induced cellular responses of macrophages and monocytes. BMB Rep 2009, 42:574-579. 10.5483/BMBRep.2009.42.9.574, 19788858.
26. Li CY, Chao LK, Wang SC, Chang HZ, Tsai ML, Fang SH, Liao PC, Ho CL, Chen ST, Cheng WC, Chiang CS, Kuo YH, Hua KF, Hsu IC. Honokiol inhibits LPS-induced maturation and inflammatory response of human monocyte-derived dendritic cells. J Cell Physiol 2011, 226:2338-2349. 10.1002/jcp.22576, 21660957.
27. Chao LK, Liao PC, Ho CL, Wang EI, Chuang CC, Chiu HW, Hung LB, Hua KF. Anti-inflammatory bioactivities of honokiol through inhibition of protein kinase C, mitogen-activated protein kinase, and the NF-kappaB pathway to reduce LPS-induced TNFalpha and NO expression. J Agric Food Chem 2011, 58:3472-3478.
28. Weng TI, Wu HY, Kuo CW, Liu SH. Honokiol rescues sepsis-associated acute lung injury and lethality via the inhibition of oxidative stress and inflammation. Intensive Care Med 2011, 37:533-541. 10.1007/s00134-010-2104-1, 21279327.
29. Li J, Shao X, Wu L, Feng T, Jin C, Fang M, Wu N, Yao H. Honokiol: an effective inhibitor of tumor necrosis factor-alpha-induced up-regulation of inflammatory cytokine and chemokine production in human synovial fibroblasts. Acta Biochim Biophys Sin (Shanghai) 2011, 43:380-386.
30. Wu F, Zhang W, Li L, Zheng F, Shao X, Zhou J, Li H. Inhibitory effects of honokiol on lipopolysaccharide-induced cellular responses and signaling events in human renal mesangial cells. Eur J Pharmacol 2011, 654:117-121. 10.1016/j.ejphar.2010.11.022, 21147091.
31. Munroe ME, Businga TR, Kline JN, Bishop GA. Anti-inflammatory effects of the neurotransmitter agonist honokiol in a mouse model of allergic asthma. J Immunol 2010, 185:5586-5597. 10.4049/jimmunol.1000630, 3197781, 20889543.
32. Chiang CK, Sheu ML, Hung KY, Wu KD, Liu SH. Honokiol, a small molecular weight natural product, alleviates experimental mesangial proliferative glomerulonephritis. Kidney Int 2006, 70:682-689. 10.1038/sj.ki.5001617, 16807544.
33. Mishra MK, Ghosh D, Duseja R, Basu A. Antioxidant potential of minocycline in Japanese Encephalitis Virus infection in murine neuroblastoma cells: correlation with membrane fluidity and cell death. Neurochem Int 2009, 54:464-470. 10.1016/j.neuint.2009.01.022, 19428790.
34. Perrella MA, Patterson C, Tan L, Yet SF, Hsieh CM, Yoshizumi M, Lee ME. Suppression of interleukin-1beta-induced nitric-oxide synthase promoter/enhancer activity by transforming growth factor-beta1 in vascular smooth muscle cells. Evidence for mechanisms other than NF-kappaB. J Biol Chem 1996, 271:13776-13780. 10.1074/jbc.271.23.13776, 8662809.
35. Pathak SK, Bhattacharyya A, Pathak S, Basak C, Mandal D, Kundu M, Basu J. Toll-like receptor 2 and mitogen- and stress-activated kinase 1 are effectors of Mycobacterium avium-induced cyclooxygenase-2 expression in macrophages. J Biol Chem 2004, 279:55127-55136. 10.1074/jbc.M409885200, 15496409.
36. Ghoshal A, Das S, Ghosh S, Mishra MK, Sharma V, Koli P, Sen E, Basu A. Proinflammatory mediators released by activated microglia induces neuronal death in Japanese encephalitis. Glia 2007, 55:483-496. 10.1002/glia.20474, 17203475.
37. Eugenin EA, Berman JW. Chemokine-dependent mechanisms of leukocyte trafficking across a model of the blood-brain barrier. Methods 2003, 29:351-361. 10.1016/S1046-2023(02)00359-6, 12725802.
38. Akira S, Taga T, Kishimoto T. Interleukin-6 in biology and medicine. Adv Immunol 1993, 54:1-78.
39. Kishimoto T. Interleukin-6 and its receptor in autoimmunity. J Autoimmun 1992, 5(Suppl A):123-132.
40. Chen CM, Liu SH, Lin-Shiau SY. Honokiol, a neuroprotectant against mouse cerebral ischaemia, mediated by preserving Na+, K + -ATPase activity and mitochondrial functions. Basic Clin Pharmacol Toxicol 2007, 101:108-116. 10.1111/j.1742-7843.2007.00082.x, 17651312.
41. 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. 10.1016/0014-5793(94)01290-3, 7805858.
42. Iadecola C, Zhang F. Permissive and obligatory roles of NO in cerebrovascular responses to hypercapnia and acetylcholine. Am J Physiol 1996, 271:R990-R1001.
43. Herschman HR. Prostaglandin synthase 2. Biochim Biophys Acta 1996, 1299:125-140.
44. Mestre JR, Mackrell PJ, Rivadeneira DE, Stapleton PP, Tanabe T, Daly JM. Redundancy in the signaling pathways and promoter elements regulating cyclooxygenase-2 gene expression in endotoxin-treated macrophage/monocytic cells. J Biol Chem 2001, 276:3977-3982. 10.1074/jbc.M005077200, 11092878.
45. Caivano M, Cohen P. Role of mitogen-activated protein kinase cascades in mediating lipopolysaccharide-stimulated induction of cyclooxygenase-2 and IL-1 beta in RAW264 macrophages. J Immunol 2000, 164:3018-3025.
46. Shen S, Yu S, Binek J, Chalimoniuk M, Zhang X, Lo SC, Hannink M, Wu J, Fritsche K, Donato R, Sun GY. Distinct signaling pathways for induction of type II NOS by IFNgamma and LPS in BV-2 microglial cells. Neurochem Int 2005, 47:298-307. 10.1016/j.neuint.2005.03.007, 15955597.
47. Kim BH, Cho JY. Anti-inflammatory effect of honokiol is mediated by PI3K/Akt pathway suppression. Acta Pharmacol Sin 2008, 29:113-122. 10.1111/j.1745-7254.2008.00725.x, 18158873.
48. Matsuda H, Kageura T, Oda M, Morikawa T, Sakamoto Y, Yoshikawa M. Effects of constituents from the bark of Magnolia obovata on nitric oxide production in lipopolysaccharide-activated macrophages. Chem Pharm Bull(Tokyo) 2001, 49:716-720.
49. Kim KR, Park KK, Chun KS, Chung WY. Honokiol inhibits the progression of collagen-induced arthritis by reducing levels of pro-inflammatory cytokines and matrix metalloproteinases and blocking oxidative tissue damage. J Pharmacol Sci 2010, 114:69-78. 10.1254/jphs.10070FP, 20703013.
50. Liou KT, Shen YC, Chen CF, Tsao CM, Tsai SK. The anti-inflammatory effect of honokiol on neutrophils: mechanisms in the inhibition of reactive oxygen species production. Eur J Pharmacol 2003, 475:19-27. 10.1016/S0014-2999(03)02121-6, 12954355.
51. Liou KT, Shen YC, Chen CF, Tsao CM, Tsai SK. Honokiol protects rat brain from focal cerebral ischemia-reperfusion injury by inhibiting neutrophil infiltration and reactive oxygen species production. Brain Res 2003, 992:159-166. 10.1016/j.brainres.2003.08.026, 14625055.
52. Cui HS, Huang LS, Sok DE, Shin J, Kwon BM, Youn UJ, Bae K. Protective action of honokiol, administered orally, against oxidative stress in brain of mice challenged with NMDA. Phytomedicine 2007, 14:696-700. 10.1016/j.phymed.2007.03.005, 17470388.