Apigenin and luteolin modulate microglial activation via inhibition of STAT1-induced CD40 expression

Journal of Neuroinflammation

Volumn 5, Issue , 2008, Pages

  Rezai Zadeh, Kavon ^a   Ehrhart, Jared ^a   Bai, Yun ^a   Sanberg, Paul R ^a   Bickford, Paula ^a,b   Tan, Jun ^a   Douglas, R Douglas ^a  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APIGENIN; CD40 ANTIGEN; FLAVONOID; GAMMA INTERFERON; INTERLEUKIN 6; LACTATE DEHYDROGENASE; LUTEOLIN; STAT1 PROTEIN; TUMOR NECROSIS FACTOR ALPHA; ANTIINFLAMMATORY AGENT; IMMUNOLOGIC FACTOR; RECOMBINANT GAMMA INTERFERON; STAT1 PROTEIN, MOUSE; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL TISSUE; ANTIGEN EXPRESSION; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL ACTIVATION; CELL LINE; CELL SURVIVAL; CONCENTRATION RESPONSE; CONTROLLED STUDY; DEGENERATIVE DISEASE; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; INHIBITION KINETICS; MICROGLIA; MOUSE; NEUROPROTECTION; NONHUMAN; PROTEIN PHOSPHORYLATION; WESTERN BLOTTING; ANIMAL; BAGG ALBINO MOUSE; BRAIN; CELL CULTURE; DOSE RESPONSE; DRUG ANTAGONISM; DRUG EFFECT; ENCEPHALITIS; FEMALE; IMMUNOLOGY; IMMUNOMODULATION; MALE; METABOLISM; PATHOPHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; ANTI-INFLAMMATORY AGENTS; ANTIGENS, CD40; APIGENIN; BRAIN; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; ENCEPHALITIS; FEMALE; IMMUNOLOGIC FACTORS; INTERFERON-GAMMA, RECOMBINANT; INTERLEUKIN-6; L-LACTATE DEHYDROGENASE; LUTEOLIN; MALE; MICE; MICE, INBRED BALB C; MICROGLIA; NEUROIMMUNOMODULATION; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR; TUMOR NECROSIS FACTOR-ALPHA;

EID: 54349113605     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-5-41     Document Type: Article

References (67)

1. Eikelenboom P Bate C Van Gool WA Hoozemans JJ Rozemuller JM Veerhuis R Williams A Neuroinflammation in Alzheimer's disease and prion disease Glia 2002, 40:232-239. 10.1002/glia.10146 12379910
2. Garden GA Microglia in human immunodeficiency virus-associated neurodegeneration Glia 2002, 40:240-251. 10.1002/glia.10155 12379911
3. Schubert P Morino T Miyazaki H Ogata T Nakamura Y Marchini C Ferroni S Cascading glia reactions: A common pathomechanism and its differentiated control by cyclic nucleotide signaling Ann N Y Acad Sci 2000, 903:24-33. 10.1111/j.1749-6632.2000.tb06346.x 10818485
4. Tan J Town T Paris D Placzek A Parker T Crawford F Yu H Humphrey J Mullan M Activation of microglial cells by the CD40 pathway: Relevance to multiple sclerosis Neuroimmunol 1999, 97:77-85. 10.1016/ S0165-5728(99)00053-3
5. Hall ED Oostveen JA Gurney ME Relationship of microglial and astrocytic activation to disease onset and progression in a transgenic model of familial ALS Glia 1998, 23:249-256. 10.1002/ (SICI)1098-1136(199807)23:3<249::AID-GLIA7>3.0.CO;2-# 9633809
6. Barger SW Harmon AD Microglial activation by Alzheimer amyloid precursor protein and modulation by apolipoprotein E Nature 1997, 388:878-881. 10.1038/42257 9278049
7. Raine C Multiple sclerosis: Immune system molecule expression in the central nervous system J Neuropathol Exp Neurol 1994, 53:328-337. 10.1097/00005072-199407000-00002 8021705
8. Dickson DW Lee SC Mattiace LA Yen SH Brosnan C Microglia and cytokines in neurological disease, with special reference to AIDS and Alzheimer's disease Glia 1993, 7:75-83. 10.1002/glia.440070113 8423065
9. Kawamata T Akiyama H Yamada T McGeer PL Immunologic reactions in amyotrophic lateral sclerosis brain and spinal cord tissue Am J Pathol 1992, 140:691-707. 1886170 1347673
10. Yamada T McGeer PL McGeer EG Relationship of complement-activated oligodendrocytes to reactive microglia and neuronal pathology in neurodegenerative disease Dementia 1991, 2:71-77. 10.1159/000107179
11. McGeer PL Itagaki S Boyes BE McGeer EG Reactive microglia are positive for HLA-DR in the substantia nigra of Parkinson's and Alzheimer's disease brains Neurology 1988, 38:1285-1291. 3399080
12. Xie Z Wei M Morgan TE Fabrizio P Han D Finch CE Longo VD Peroxynitrite mediates neurotoxicity of amyloid β-peptide1-42-and lipopolysaccharide-activated microglia J Neurosci 2002, 22:3484-3492. 11978825
13. McGuire SO Ling ZD Lipton JW Sortwell CE Collier TJ Carvey PM Tumor necrosis factor alpha is toxic to embryonic mesencephalic dopamine neurons Exp Neurol 2001, 169:219-230. 10.1006/exnr.2001.7688 11358437
14. Jeohn G-H Kong L-Y Wilson B Hudson P Hong J-S Synergistic neurotoxic effects of combined treatments with cytokines in murine primary mixed neuron/glia cultures J Neuroimmuno 1998, 85:1-10. 10.1016/ S0165-5728(97)00204-X
15. Chao CC Hu S Ehrlich L Peterson PK Interleukin-1 and tumor necrosis factor-α synergistically mediate neurotoxicity: Involvement of nitric oxide and of N-methyl-D-aspartate receptors Brain Behav Immun 1995, 9:355-365. 10.1006/brbi.1995.1033 8903852
16. Boje KM Arora PK Microglial-produced nitric oxide and reactive nitrogen oxides mediate neuronal cell death Brain Res 1992, 587:250-6. 10.1016/ 0006-8993(92)91004-X 1381982
17. Chao CC Hu S Molitor TW Shaskan EG Peterson PK Activated microglia mediate neuronal cell injury via a nitric oxide mechanism J Immunol 1992, 149:2736-2741. 1383325
18. Streit WJ Microglia and neuroprotection: Implications for Alzheimer's disease Brain Res Brain Res Rev 2005, 48:234-9. 10.1016/ j.brainresrev.2004.12.013 15850662
19. Alderson MR Armitage RJ Tough TW Strockbine L Fanslow WC Spriggs MK CD40 expression by human monocytes: Regulation by cytokines and activation of monocytes by the ligand for CD40 J Exp Med 1993, 178:669-74. 2191134 7688031 10.1084/jem.178.2.669
20. van Kooten C Banchereau J CD40-CD40 ligand J Leukoc Biol 2000, 67:2-17. 10647992
21. Grewal IS Flavell RA CD40 and CD154 in cell-mediated immunity Annu Rev Immunol 1998, 16:111-135. 10.1146/annurev.immunol.16.1.111 9597126
22. Nguyen VT Walker WS Benveniste EN, Post-transcriptional inhibition of CD40 gene expression in microglia by transforming growth factor-beta Eur J Immunol 1998, 28:2537-2548. 10.1002/ (SICI)1521-4141(199808)28:08<2537::AID-IMMU2537>3.0.CO;2-1 9710231
23. Boehm U Klamp T Groot M Howard JC Cellular responses to interferon-gamma Annu Rev Immunol 1997, 15:749-795. 10.1146/annurev.immunol.15.1.749 9143706
24. Seder Paul RA Seder Paul WE Acquisition of lymphokine-producing phenotype by CD4+ T cells Annu Rev Immunol 1994, 12:635-673. 10.1146/ annurev.iy.12.040194.003223 7912089
25. Nguyen VT Benveniste EN Involvement of STAT-1 and ets family members in interferon-gamma induction of CD40 transcription in microglia/ macrophages J Biol Chem 2000, 275:23674-84. 10.1074/jbc.M002482200 10823830
26. Leonard WJ O'Shea JJ Jaks and STATs: Biological implications Annu Rev Immunol 1998, 16:293-322. 10.1146/annurev.immunol.16.1.293 9597132
27. Townsend KP Town T Mori T Lue LF Shytle D Sanberg PR Morgan D Fernandez F Flavell RA Tan J CD40 signaling regulates innate and adaptive activation of microglia in response to amyloid beta-peptide Eur J Immunol 2005, 35:901-10. 10.1002/eji.200425585 15688347
28. Townsend KP Shytle DR Bai Y San N Zeng J Freeman M Mori T Fernandez F Morgan D Sanberg P Tan J Lovastatin modulation of microglial activation via suppression of functional CD40 expression J Neurosci Res 2004, 78:167-76. 10.1002/jnr.20234 15378516
29. Dai Q Borenstein AR Wu Y Jackson JC Larson EB Fruit and vegetable juices and Alzheimer's disease: The Kame Project Am J Med 2006, 119:751-9. 2266591 16945610 10.1016/j.amjmed.2006.03.045
30. Genkinger JM Platz EA Hoffman SC Comstock GW Helzlsouer KJ Fruit, vegetable, and antioxidant intake and all-cause, cancer, and cardiovascular disease mortality in a community-dwelling population in Washington County, Maryland Am J Epidemiol 2004, 160:1223-33. 15583375
31. Laurin D Masaki KH Foley DJ White LR Launer LJ Midlife Dietary Intake of Antioxidants and Risk of Late-Life Incident Dementia: The Honolulu-Asia Aging Study Am J Epidemiol 2004, 159:959-967. 10.1093/aje/kwh124 15128608
32. Bastianetto S Red wine consumption and brain aging Nutrition 2002, 18:432-3. 10.1016/S0899-9007(01)00745-6 11985952
33. Sun AY Simonyi A Sun GY The "French Paradox" and beyond: neuroprotective effects of polyphenols Free Radic Biol Med 2002, 32:314-8. 10.1016/S0891-5849(01)00803-6 11841921
34. Sampson L Rimm E Hollman PC de Vries JH Katan MB Flavonol and flavone intakes in US health professionals J Am Diet Assoc 2002, 102:1414-20. 10.1016/S0002-8223(02)90314-7 12396158
35. Nielsen SE Young JF Daneshvar B Lauridsen ST Knuthsen P Sandstrom B Dragsted LO Effect of parsley (Petroselinum crispum) intake on urinary apigenin excretion, blood antioxidant enzymes and biomarkers for oxidative stress in human subjects Br J Nutr 1999, 81:447-55. 10615220
36. van Acker SA Berg van den DJ Tromp MN Structural aspects of antioxidant activity of flavonoids Free Rad Biol Med 1996, 20:331-342. 10.1016/ 0891-5849(95)02047-0 8720903
37. Saija A Scalese M Lanza M Marzullo D Bonina F Flavonoids as antioxidant agents: Importance of their interaction with biomembranes Free Rad Biol Med 1995, 19:481-486. 10.1016/0891-5849(94)00240-K 7590397
38. Kanadaswami C Lee LT Lee PP Hwang JJ Ke FC Huang YT Lee MT The antitumor activities of flavonoids In Vivo 2005, 19:895-909. 16097445
39. Ren W Qiao Z Wang H Zhu L Zhang L Flavonoids: Promising anticancer agents Med Res Rev 2003, 23:519-34. 10.1002/med.10033 12710022
40. Ferrandiz ML Gil B Sanz MJ Effect of bakuchiol on leukocyte functions and some inflammatory responses in mice J Pharm Pharmacol 1996, 48:975-80. 8910867
41. Friesenecker B Tsai AG Allegra C Intaglietta M Oral administration of purified micronized flavonoid fraction suppresses leukocyte adhesion in ischemia-reperfusion injury: In vivo observations in the hamster skin fold Int J Microcirc Clin Exp 1994, 14:50-5. 7960444
42. Bennett JP Gomperts BD Wollenweber E Inhibitory effects of natural flavonoids on secretion from mast cells and neutrophils Arzneimittelforschung 1981, 31:433-7. 6164375
43. Yoon MS Lee JS Choi BM Jeong YI Lee CM Park JH Moon Y Sung SC Lee SK Chang YH Chung HY Park YM Apigenin inhibits immunostimulatory function of dendritic cells: Implication of immunotherapeutic adjuvant Mol Pharmacol 2006, 70(3):1033-1044. 10.1124/mol.106.024547 16782805
44. Hirano T Arimitsu J Higa S Naka T Ogata A Shima Y Fujimoto M Yamadori T Ohkawara T Kuwabara Y Kawai M Kawase I Tanaka T Luteolin, a flavonoid, inhibits CD40 ligand expression by activated human basophils Int Arch Allergy Immunol 2006, 40:150-6. 10.1159/000092554
45. Ueda H Yamazaki C Yamazaki M A hydroxyl group of flavonoids affects oral anti-inflammatory activity and inhibition of systemic tumor necrosis factor-alpha production Biosci Biotechnol Biochem 2004, 68:119-25. 10.1271/bbb.68.119 14745173
46. Smolinski AT Pestka JJ Modulation of lipopolysaccharide-induced proinflammatory cytokine production in vitro and in vivo by the herbal constituents apigenin (chamomile), ginsenoside Rb(1) (ginseng) and parthenolide (feverfew) Food Chem Toxicol 2003, 41:1381-90. 10.1016/ S0278-6915(03)00146-7 12909272
47. Raso GM Meli R Di Carlo G Pacilio M Di Carlo R Inhibition of inducible nitric oxide synthase and cyclooxygenase-2 expression by flavonoids in macrophage J774A.1 Life Sci 2001, 68:921-31. 10.1016/ S0024-3205(00)00999-1 11213362
48. Liang YC Tsai SH Tsai DC Lin-Shiau SY Lin JK Suppression of inducible cyclooxygenase and nitric oxide synthase through activation of peroxisome proliferator-activated receptor-gamma by flavonoids in mouse macrophages FEBS Lett 2001, 496:12-8. 10.1016/S0014-5793(01)02393-6 11343698
49. Gerritsen ME Carley WW Ranges GE Shen CP Phan SA Ligon GF Perry CA Flavonoids inhibit cytokine-induced endothelial cell adhesion protein gene expression Am J Pathol 1995, 147:278-92. 1869822 7543732
50. Tan J Town T Saxe M Paris D Wu Y Mullan M, Ligation of microglial CD40 results in p44/42 mitogen-activated protein kinase-dependent TNF-alpha production that is opposed by TGF-beta 1 and IL-10 J Immunol 1999, 163:6614-21. 10586056
51. Corradin SB Mauël J Donini SD Quattrocchi E Ricciardi-Castagnoli P Inducible nitric oxide synthase activity of cloned murine microglial cells Glia 1993, 7:255-62. 10.1002/glia.440070309 7681038
52. Matsuo M Sasaki N Saga K Kaneko T Cytotoxicity of flavonoids toward cultured normal human cells Biol Pharm Bull 2005, 28:253-9. 10.1248/ bpb.28.253 15684479
53. Kovarik P Mangold M Ramsauer K Specificity of signaling by STAT1 depends on SH2 and C-terminal domains that regulate Ser727 phosphorylation, differentially affecting specific target gene expression EMBO J 2001, 20:91-100. 140204 11226159 10.1093/emboj/20.1.91
54. Goh KC Haque SJ Williams BR p38 MAP kinase is required for STAT1 serine phosphorylation and transcriptional activation induced by interferons EMBO J 1999, 18:5601-8. 1171628 10523304 10.1093/emboj/18.20.5601
55. Chen D Daniel KG Chen MS Kuhn DJ Landis-Piwowar KR Dou QP Dietary flavonoids as proteasome inhibitors and apoptosis inducers in human leukemia cells Biochem Pharmacol 2005, 69:1421-32. 10.1016/ j.bcp.2005.02.022 15857606
56. Zheng PW Chiang LC Lin CC Apigenin induced apoptosis through p53-dependent pathway in human cervical carcinoma cells Life Sci 2005, 76:1367-79. 10.1016/j.lfs.2004.08.023 15670616
57. Elsisi NS Darling-Reed S Lee EY Oriaku ET Soliman KF Ibuprofen and apigenin induce apoptosis and cell cycle arrest in activated microglia Neurosci Lett 2005, 375:91-6. 10.1016/j.neulet.2004.10.087 15670648
58. Townsend PA Scarabelli TM Davidson SM Knight RA Latchman DS Stephanou A STAT-1 interacts with p53 to enhance DNA damage-induced apoptosis J Biol Chem 2004, 279:5811-20. 10.1074/jbc.M302637200 14602726
59. Stephanou A Scarabelli TM Brar BK Nakanishi Y Matsumura M Knight RA Latchman DS Induction of apoptosis and Fas receptor/Fas ligand expression by ischemia/reperfusion in cardiac myocytes requires serine 727 of the STAT-1 transcription factor but not tyrosine 701 J Biol Chem 2001, 276:28340-7. 10.1074/jbc.M101177200 11309387
60. Kumar A Commane M Flickinger TW Horvath CM Stark GR Defective TNF-alpha-induced apoptosis in STAT1-null cells due to low constitutive levels of caspases Science 1997, 278:1630-2. 10.1126/ science.278.5343.1630 9374464
61. Tan J Town T Mori T Obregon D Wu Y DelleDonne A Rojiani A Crawford F Flavell RA Mullan M CD40 is expressed and functional on neuronal cells EMBO J 2002, 21:643-52. 125862 11847112 10.1093/emboj/21.4.643
62. Nguyen H Ramana CV Bayes J Stark GR Roles of phosphatidylinositol 3-kinase in interferon-gamma-dependent phosphorylation of STAT1 on serine 727 and activation of gene expression J Biol Chem 2001, 276:33361-8. 10.1074/jbc.M105070200 11438544
63. Irie-Sasaki J Sasaki T Matsumoto W Opavsky A Cheng M Welstead G Griffiths E Krawczyk C Richardson CD Aitken K Iscove N Koretzky G Johnson P Liu P Rothstein DM Penninger JM CD45 is a JAK phosphatase and negatively regulates cytokine receptor signaling Nature 2001, 409:349-54. 10.1038/35053086 11201744
64. Manach C Williamson G Morand C Scalbert A Remesy C Bioavailability and bioefficacy of polyphenols in humans. I. Review of 97 bioavailability studies Am J Clin Nutr 2005, 81:230S-42S. 15640486
65. Gradolatto A Basly JP Berges R Teyssier C Chagnon MC Siess MH Canivenc-Lavier MC Pharmacokinetics and metabolism of apigenin in female and male rats after a single oral administration Drug Metab Dispos 2005, 33:49-54. 10.1124/dmd.104.000893 15466493
66. Gradolatto A Canivenc-Lavier MC Basly JP Siess MH Teyssier C Metabolism of apigenin by rat liver phase I and phase ii enzymes and by isolated perfused rat liver Drug Metab Dispos 2004, 32:58-65. 10.1124/dmd.32.1.58 14709621
67. Li LP Jiang HD Determination and assay validation of luteolin and apigenin in human urine after oral administration of tablet of Chrysanthemum morifolium extract by HPLC J Pharm Biomed Anal 2006, 41:261-5. 10.1016/j.jpba.2005.10.019 16318906