Krüppel-like factor 4, a novel transcription factor regulates microglial activation and subsequent neuroinflammation

Journal of Neuroinflammation

Volumn 7, Issue , 2010, Pages

  Kaushik, Deepak K ^a   Gupta, Malvika ^a   Das, Sulagna ^a   Basu, Anirban ^a  

^a NATIONAL BRAIN RESEARCH CENTRE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; CYCLOOXYGENASE 2; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 6; KRUPPEL LIKE FACTOR 4; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; NITRIC OXIDE; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE; KRUPPEL LIKE FACTOR; LIPOPOLYSACCHARIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENCEPHALITIS; IN VITRO STUDY; MICROGLIA; MOUSE; NONHUMAN; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SALMONELLA ENTERICA; ANIMAL; CELL CULTURE; CELL LINE; DOSE RESPONSE; DRUG EFFECT; GEL MOBILITY SHIFT ASSAY; GENETICS; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MACROPHAGE ACTIVATION; METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CELL LINE; CELLS, CULTURED; CYCLOOXYGENASE 2; CYTOKINES; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ENCEPHALITIS; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; KRUPPEL-LIKE TRANSCRIPTION FACTORS; LIPOPOLYSACCHARIDES; MACROPHAGE ACTIVATION; MICE; MICROGLIA; NF-KAPPA B; NITRIC OXIDE SYNTHASE TYPE II; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 77957922334     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-7-68     Document Type: Article

References (64)

1. Cerciat M, Unkila M, Garcia-Segura LM, Arevalo MA. Selective estrogen receptor modulators decrease the production of interleukin-6 and interferon-gamma-inducible protein-10 by astrocytes exposed to inflammatory challenge in vitro. Glia 2010, 58:93-102. 10.1002/glia.20904, 19533603.
2. Carson MJ, Thrash JC, Lo D. Analysis of microglial gene expression: identifying targets for CNS neurodegenerative and autoimmune disease. Am J Pharmacogenomics 2004, 4:321-30. 10.2165/00129785-200404050-00005, 15462610.
3. Kreutzberg GW. Microglia: a sensor for pathological events in the CNS. Trends Neurosci 1996, 19:312-8. 10.1016/0166-2236(96)10049-7, 8843599.
4. Beyer M, Gimsa U, Eyupoglu IY, Hailer NP, Nitsch R. Phagocytosis of neuronal or glial debris by microglial cells: upregulation of MHC class II expression and multinuclear giant cell formation in vitro. Glia 2000, 31:262-6. 10.1002/1098-1136(200009)31:3<262::AID-GLIA70>3.0.CO;2-2, 10941152.
5. Brown GC, Neher JJ. Inflammatory Neurodegeneration and Mechanisms of Microglial Killing of Neurons. Mol Neurobiol 2010, 41(2-3):242-7. 10.1007/s12035-010-8105-9, 20195798.
6. Perry VH, Nicoll JA, Holmes C. Microglia in neurodegenerative disease. Nat Rev Neurol 2010, 6:193-201. 10.1038/nrneurol.2010.17, 20234358.
7. Carson MJ. Microglia as liaisons between the immune and central nervous systems: functional implications for multiple sclerosis. Glia 2002, 40:218-31. 10.1002/glia.10145, 2693029, 12379909.
8. Kim YS, Joh TH. Microglia, major player in the brain inflammation: their roles in the pathogenesis of Parkinson's disease. Exp Mol Med 2006, 38:333-47.
9. Dinarello CA. The interleukin-1 family: 10 years of discovery. Faseb J 1994, 8:1314-25.
10. Takeuchi O, Hoshino K, Kawai T, Sanjo H, Takada H, Ogawa T, Takeda K, Akira S. Differential roles of TLR2 and TLR4 in recognition of gram-negative and gram-positive bacterial cell wall components. Immunity 1999, 11:443-51. 10.1016/S1074-7613(00)80119-3, 10549626.
11. Qureshi ST, Gros P, Malo D. Host resistance to infection: genetic control of lipopolysaccharide responsiveness by TOLL-like receptor genes. Trends Genet 1999, 15:291-4. 10.1016/S0168-9525(99)01782-5, 10431187.
12. Zhang FX, Kirschning CJ, Mancinelli R, Xu XP, Jin Y, Faure E, Mantovani A, Rothe M, Muzio M, Arditi M. Bacterial lipopolysaccharide activates nuclear factor-kappaB through interleukin-1 signaling mediators in cultured human dermal endothelial cells and mononuclear phagocytes. J Biol Chem 1999, 274:7611-4. 10.1074/jbc.274.12.7611, 10075645.
13. Doyle SL, Jefferies CA, O'Neill LA. Bruton's tyrosine kinase is involved in p65-mediated transactivation and phosphorylation of p65 on serine 536 during NFkappaB activation by lipopolysaccharide. J Biol Chem 2005, 280:23496-501. 10.1074/jbc.C500053200, 15849198.
14. 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, 480-481:243-68.
15. 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, 275:34035-40. 10.1074/jbc.M007386200, 10952994.
16. 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.
17. SenBanerjee S, Lin Z, Atkins GB, Greif DM, Rao RM, Kumar A, Feinberg MW, Chen Z, Simon DI, Luscinskas FW, Michel TM, Gimbrone MA, Garcia-Cardena G, Jain MK. KLF2 Is a novel transcriptional regulator of endothelial proinflammatory activation. J Exp Med 2004, 199:1305-15. 10.1084/jem.20031132, 2211816, 15136591.
18. 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, 280:38247-58. 10.1074/jbc.M509378200, 16169848.
19. 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, 282:13769-79. 10.1074/jbc.M700078200, 17339326.
20. Shields JM, Christy RJ, Yang VW. Identification and characterization of a gene encoding a gut-enriched Kruppel-like factor expressed during growth arrest. J Biol Chem 1996, 271:20009-17. 10.1074/jbc.271.33.20009, 2330254, 8702718.
21. 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, 129:2619-28. 2225535, 12015290.
22. Segre JA, Bauer C, Fuchs E. Klf4 is a transcription factor required for establishing the barrier function of the skin. Nat Genet 1999, 22:356-60. 10.1038/11926, 10431239.
23. 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, 278:2101-5. 10.1074/jbc.M211027200, 2229830, 12427745.
24. Yoon HS, Yang VW. Requirement of Kruppel-like factor 4 in preventing entry into mitosis following DNA damage. J Biol Chem 2004, 279:5035-41. 10.1074/jbc.M307631200, 1262649, 14627709.
25. Li Y, McClintick J, Zhong L, Edenberg HJ, Yoder MC, Chan RJ. Murine embryonic stem cell differentiation is promoted by SOCS-3 and inhibited by the zinc finger transcription factor Klf4. Blood 2005, 105:635-7. 10.1182/blood-2004-07-2681, 15358627.
26. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006, 126:663-76. 10.1016/j.cell.2006.07.024, 16904174.
27. Kuhn DM, Francescutti-Verbeem DM, Thomas DM. Dopamine quinones activate microglia and induce a neurotoxic gene expression profile: relationship to methamphetamine-induced nerve ending damage. Ann N Y Acad Sci 2006, 1074:31-41. 10.1196/annals.1369.003, 17105901.
28. Liu J, Liu Y, Zhang H, Chen G, Wang K, Xiao X. KLF4 promotes the expression, translocation, and releas eof HMGB1 in RAW264.7 macrophages in response to LPS. Shock 2008, 30:260-6.
29. 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, 284:35471-8. 10.1074/jbc.M109.046813, 19858207.
30. 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, 180:5645-52.
31. Dutta K, Ghosh D, Nazmi A, Kumawat KL, Basu A. A common carcinogen benzo[a]pyrene causes neuronal death in mouse via microglial activation. PLoS One 2010, 5:e9984. 10.1371/journal.pone.0009984, 2848611, 20376308.
32. Basu A, Krady JK, Enterline JR, Levison SW. Transforming growth factor beta1 prevents IL-1beta-induced microglial activation, whereas TNFalpha- and IL-6-stimulated activation are not antagonized. Glia 2002, 40:109-20. 10.1002/glia.10118, 12237848.
33. 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, 271:13776-80. 10.1074/jbc.271.23.13776, 8662809.
34. 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, 279:55127-36. 10.1074/jbc.M409885200, 15496409.
35. 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, 55:483-96. 10.1002/glia.20474, 17203475.
36. Das S, Ghosh D, Basu A. Japanese encephalitis virus induce immuno-competency in neural stem/progenitor cells. PLoS One 2009, 4:e8134. 10.1371/journal.pone.0008134, 2780913, 19956550.
37. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-8. 10.1006/meth.2001.1262, 11846609.
38. Soldan SS, Alvarez Retuerto AI, Sicotte NL, Voskuhl RR. Dysregulation of IL-10 and IL-12p40 in secondary progressive multiple sclerosis. J Neuroimmunol 2004, 146:209-15. 10.1016/j.jneuroim.2003.10.033, 14698865.
39. Shukla S, Gupta S. Suppression of constitutive and tumor necrosis factor alpha-induced nuclear factor (NF)-kappaB activation and induction of apoptosis by apigenin in human prostate carcinoma PC-3 cells: correlation with down-regulation of NF-kappaB-responsive genes. Clin Cancer Res 2004, 10:3169-78. 10.1158/1078-0432.CCR-03-0586, 15131058.
40. Eugenin EA, Berman JW. Chemokine-dependent mechanisms of leukocyte trafficking across a model of the blood-brain barrier. Methods 2003, 29:351-61. 10.1016/S1046-2023(02)00359-6, 12725802.
41. Akira S, Taga T, Kishimoto T. Interleukin-6 in biology and medicine. Adv Immunol 1993, 54:1-78. full_text, 8379461.
42. Kishimoto T. Interleukin-6 and its receptor in autoimmunity. J Autoimmun 1992, 5(Suppl A):123-32. 10.1016/0896-8411(92)90027-N, 1380241.
43. Fialkow L, Wang Y, Downey GP. Reactive oxygen and nitrogen species as signaling molecules regulating neutrophil function. Free Radic Biol Med 2007, 42:153-64. 10.1016/j.freeradbiomed.2006.09.030, 17189821.
44. Minghetti L, Ajmone-Cat MA, De Berardinis MA, De Simone R. Microglial activation in chronic neurodegenerative diseases: roles of apoptotic neurons and chronic stimulation. Brain Res Brain Res Rev 2005, 48:251-6. 10.1016/j.brainresrev.2004.12.015, 15850664.
45. Waetzig V, Czeloth K, Hidding U, Mielke K, Kanzow M, Brecht S, Goetz M, Lucius R, Herdegen T, Hanisch UK. c-Jun N-terminal kinases (JNKs) mediate pro-inflammatory actions of microglia. Glia 2005, 50:235-46. 10.1002/glia.20173, 15739188.
46. 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, 55:453-62. 10.1002/glia.20467, 2871685, 17203472.
47. 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.
48. Ledeboer A, Breve JJ, Wierinckx A, van der Jagt S, Bristow AF, Leysen JE, Tilders FJ, Van Dam AM. Expression and regulation of interleukin-10 and interleukin-10 receptor in rat astroglial and microglial cells. Eur J Neurosci 2002, 16:1175-85. 10.1046/j.1460-9568.2002.02200.x, 12405978.
49. Sakurai H, Chiba H, Miyoshi H, Sugita T, Toriumi W. IkappaB kinases phosphorylate NF-kappaB p65 subunit on serine 536 in the transactivation domain. J Biol Chem 1999, 274:30353-6. 10.1074/jbc.274.43.30353, 10521409.
50. Medugno L, Florio F, Cesaro E, Grosso M, Lupo A, Izzo P, Costanzo P. Differential expression and cellular localization of ZNF224 and ZNF255, two isoforms of the Kruppel-like zinc-finger protein family. Gene 2007, 403:125-31. 10.1016/j.gene.2007.07.036, 17900823.
51. Huang Z, Philippin B, O'Leary E, Bonventre JV, Kriz W, Witzgall R. Expression of the transcriptional repressor protein Kid-1 leads to the disintegration of the nucleolus. J Biol Chem 1999, 274:7640-8. 10.1074/jbc.274.12.7640, 10075651.
52. Yano K, Ueki N, Oda T, Seki N, Masuho Y, Muramatsu M. Identification and characterization of human ZNF274 cDNA, which encodes a novel kruppel-type zinc-finger protein having nucleolar targeting ability. Genomics 2000, 65:75-80. 10.1006/geno.2000.6140, 10777669.
53. Evans PM, Zhang W, Chen X, Yang J, Bhakat KK, Liu C. Kruppel-like factor 4 is acetylated by p300 and regulates gene transcription via modulation of histone acetylation. J Biol Chem 2007, 282:33994-4002. 10.1074/jbc.M701847200, 17908689.
54. Iadecola C, Zhang F. Permissive and obligatory roles of NO in cerebrovascular responses to hypercapnia and acetylcholine. Am J Physiol 1996, 271:R990-1001.
55. Brown GC, Cooper CE. Nanomolar concentrations of nitric oxide reversibly inhibit synaptosomal respiration by competing with oxygen at cytochrome oxidase. FEBS Lett 1994, 356:295-8. 10.1016/0014-5793(94)01290-3, 7805858.
56. Block ML, Zecca L, Hong JS. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat Rev Neurosci 2007, 8:57-69. 10.1038/nrn2038, 17180163.
57. Herschman HR. Prostaglandin synthase 2. Biochim Biophys Acta 1996, 1299:125-40.
58. Tanabe T, Tohnai N. Cyclooxygenase isozymes and their gene structures and expression. Prostaglandins Other Lipid Mediat 2002, 68-69:95-114. 10.1016/S0090-6980(02)00024-2, 12432912.
59. 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, 276:3977-82. 10.1074/jbc.M005077200, 11092878.
60. de Oliveira AC, Candelario-Jalil E, Bhatia HS, Lieb K, Hull M, Fiebich BL. Regulation of prostaglandin E2 synthase expression in activated primary rat microglia: evidence for uncoupled regulation of mPGES-1 and COX-2. Glia 2008, 56:844-55. 10.1002/glia.20658, 18383341.
61. 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, 164:3018-25.
62. Shao J, Yang VW, Sheng H. Prostaglandin E2 and Kruppel-like transcription factors synergistically induce the expression of decay-accelerating factor in intestinal epithelial cells. Immunology 2008, 125:397-407. 10.1111/j.1365-2567.2008.02847.x, 2669143, 18435741.
63. Cullingford TE, Butler MJ, Marshall AK, Tham el L, Sugden PH, Clerk A. Differential regulation of Kruppel-like factor family transcription factor expression in neonatal rat cardiac myocytes: effects of endothelin-1, oxidative stress and cytokines. Biochim Biophys Acta 2008, 1783:1229-36. 10.1016/j.bbamcr.2008.03.007, 2396231, 18406357.
64. Petrova TV, Akama KT, Van Eldik LJ. Cyclopentenone prostaglandins suppress activation of microglia: down-regulation of inducible nitric-oxide synthase by 15-deoxy-Delta12,14-prostaglandin J2. Proc Natl Acad Sci USA 1999, 96:4668-73. 10.1073/pnas.96.8.4668, 16390, 10200320.