Luteolin downregulates TLR4, TLR5, NF-κB and p-p38MAPK expression, upregulates the p-ERK expression, and protects rat brains against focal ischemia

Brain Research

Volumn 1448, Issue , 2012, Pages 71-81

  Qiao, Huimin ^a   Zhang, Xiangjian ^a,b,c   Zhu, Chunhua ^a,b,c   Dong, Lipeng ^a   Wang, Lina ^a   Zhang, Xiaolin ^a   Xing, Yinxue ^a   Wang, Chaohui ^a   Ji, Ye ^a   Cao, Xiaoyun ^a  

^a HEBEI MEDICAL UNIVERSITY   (China)

^b Hebei Institute of Cardio Cerebral Vascular Diseases   (China)

^c Hebei Key Laboratory for Neurology   (China)

Author keywords

Inflammation; Ischemic stroke; Luteolin; Neuroprotection

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LUTEOLIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 14; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 5;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN EDEMA; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; BRAIN WATER; CONTROLLED STUDY; DOWN REGULATION; DRUG MEGADOSE; IMMUNOHISTOCHEMISTRY; MALE; NEUROLOGIC DISEASE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; STROKE; UPREGULATION; WATER CONTENT; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; BRAIN; BRAIN EDEMA; BRAIN ISCHEMIA; CEREBRAL INFARCTION; DOWN-REGULATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; INFARCTION, MIDDLE CEREBRAL ARTERY; LUTEOLIN; MALE; MOVEMENT DISORDERS; NERVOUS SYSTEM DISEASES; NEUROPROTECTIVE AGENTS; NF-KAPPA B; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; REAL-TIME POLYMERASE CHAIN REACTION; STROKE; TOLL-LIKE RECEPTOR 4; TOLL-LIKE RECEPTOR 5; UP-REGULATION;

RATTUS;

EID: 84862788886     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2012.02.003     Document Type: Article

References (60)

1. Abreu, M.T., Arditi, M., 2004. Innate immunity and toll-like receptors: clinical implications of basic science research. J. Pediatr. 144, 421-429. (Pubitemid 38457342)
2. Akira, S., 2003. Toll-like receptor signaling. J. Biol. Chem. 278, 38105-38108. (Pubitemid 37221695)
3. Akira, S., Takeda, K., 2004. Toll-like receptor signalling. Nat. Rev. Immunol. 4, 499-511. (Pubitemid 38931765)
4. Akira, S., Uematsu, S., Takeuchi, O., 2006. Pathogen recognition and innate immunity. Cell 124, 783-801. (Pubitemid 43261452)
5. Allan, S.M., Rothwell, N.J., 2001. Cytokines and acute neurodegeneration. Nat. Rev. Neurosci. 2, 734-744. (Pubitemid 33674819)
6. Armstrong, S.C., Delacey, M., Ganote, C.E., 1999. Phosphorylation state of hsp27 and p38 MAPK during preconditioning and protein phosphatase inhibitor protection of rabbit cardiomyocytes. J. Mol. Cell. Cardiol. 31, 555-567. (Pubitemid 29121642)
7. Barone, F.C., Irving, E.A., Ray, A.M., Lee, J.C., Kassis, S., Kumar, S., Badger, A.M., White, R.F., McVey, M.J., Legos, J.J., Erhardt, J.A., Nelson, A.H., Ohlstein, E.H., Hunter, A.J., Ward, K., Smith, B.R., Adams, J.L., Parsons, A.A., 2001. SB 239063, a second-generation p38 mitogen-activated protein kinase inhibitor, reduces brain injury and neurological deficits in cerebral focal ischemia. J. Pharmacol. Exp. Ther. 296, 312-321. (Pubitemid 32112455)
8. Bederson, J.B., Pitts, L.H., Germano, S.M., Nishimura, M.C., Davis, R.L., Bartkowski, H.M., 1986. Evaluation of 2,3,5-triphenyltetrazolium chloride as a stain for detection and quantification of experimental cerebral infarction in rats. Stroke 17, 1304-1308. (Pubitemid 17008976)
9. Blanco,A.M., Pascual, M.,Valles, S.L.,Guerri, C., 2004. Ethanol-induced iNOS and COX-2 expression in cultured astrocytes viaNF-kappa B. Neuroreport 15, 681-685. (Pubitemid 38457160)
10. Blohmke, C.J., Park, J., Hirschfeld, A.F., Victor, R.E., Schneiderman, J., Stefanowicz, D., Chilvers, M.A., Durie, P.R., Corey, M., Zielenski, J., Dorfman, R., Sandford, A.J., Daley, D., Turvey, S.E., TLR5 as an anti-inflammatory target and modifier gene in cystic fibrosis. J. Immunol. 185, 7731-7738.
11. Bsibsi, M., Ravid, R., Gveric, D., van Noort, J.M., 2002. Broad expression of Toll-like receptors in the human central nervous system. J. Neuropathol. Exp. Neurol. 61, 1013-1021. (Pubitemid 35278723)
12. Caso, J.R., Pradillo, J.M., Hurtado, O., Lorenzo, P., Moro, M.A., Lizasoain, I., 2007. Toll-like receptor 4 is involved in brain damage and inflammation after experimental stroke. Circulation 115, 1599-1608. (Pubitemid 46648645)
13. Chen, C.C., Chow, M.P., Huang, W.C., Lin, Y.C., Chang, Y.J., 2004. Flavonoids inhibit tumor necrosis factor-alpha-induced up-regulation of intercellular adhesion molecule-1 (ICAM-1) in respiratory epithelial cells through activator protein-1 and nuclear factor-kappaB: structure-activity relationships. Mol. Pharmacol. 66, 683-693.
14. Chen, Z.B., Huang, D.Q., Niu, F.N., Zhang, X., Li, E.G., Xu, Y., 2010. Human urinary kallidinogenase suppresses cerebral inflammation in experimental stroke and downregulates nuclear factor-kappaB. J. Cereb. Blood Flow Metab. 30, 1356-1365.
15. Choi, B.M., Lim, D.W., Lee, J.A., Gao, S.S., Kwon, D.Y., Kim, B.R., 2008. Luteolin suppresses cisplatin-induced apoptosis in auditory cells: possible mediation through induction of heme oxygenase-1 expression. J. Med. Food 11, 230-236. (Pubitemid 351948178)
16. Coleta, M., Campos, M.G., Cotrim, M.D., Lima, T.C., Cunha, A.P., 2008. Assessment of luteolin (3′,4′,5,7-tetrahydroxyflavone) neuropharmacological activity. Behav. Brain Res. 189, 75-82.
17. Cui, L., Zhang, X., Yang, R., Liu, L., Wang, L., Li, M., Du, W., 2010. Baicalein is neuroprotective in rat MCAO model: role of 12/15-lipoxygenase, mitogen-activated protein kinase and cytosolic phospholipase A2. Pharmacol. Biochem. Behav. 96, 469-475.
18. Davis, R.J., 1994. MAPKs: new JNK expands the group. Trends Biochem. Sci. 19, 470-473. (Pubitemid 24342759)
19. De Keulenaer, G.W., Ushio-Fukai, M., Yin, Q., Chung, A.B., Lyons, P.R., Ishizaka, N., Rengarajan, K., Taylor, W.R., Alexander, R.W., Griendling, K.K., 2000. Convergence of redox-sensitive and mitogen-activated protein kinase signaling pathways in tumor necrosis factor-alpha-mediated monocyte chemoattractant protein-1 induction in vascular smoothmuscle cells. Arterioscler. Thromb. Vasc. Biol. 20, 385-391. (Pubitemid 30086094)
20. Fan, H., Cook, J.A., 2004. Molecular mechanisms of endotoxin tolerance. J. Endotoxin Res. 10, 71-84.
21. Fan, H., Li, L., Zhang, X., Liu, Y., Yang, C., Yang, Y., Yin, J., 2009. Oxymatrine downregulates TLR4, TLR2, MyD88, and NF-kappaB and protects rat brains against focal ischemia. Mediators Inflamm. 2009, 704706.
22. Gutiérrez-Venegas, G., Kawasaki-Cárdenas, P., Arroyo-Cruz, S.R., Maldonado-Frías, S., 2006. Luteolin inhibits lipopolysaccharide actions on human gingival fibroblasts. Eur. J. Pharmacol. 541, 95-105. (Pubitemid 44192369)
23. Hatashita, S., Hoff, J.T., Salamat, S.M., 1988. Ischemic brain edema and the osmotic gradient between blood and brain. J. Cereb. Blood Flow Metab. 8, 552-559.
24. Hayashi, F., Smith, K.D., Ozinsky, A., Hawn, T.R., Yi, E.C., Goodlett, D.R., Eng, J.K., Akira, S., Underhill, D.M., Aderem, A., 2001. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410, 1099-1103. (Pubitemid 32391041)
25. Hicks, A., Jolkkonen, J., 2009. Challenges and possibilities of intravascular cell therapy in stroke. Acta Neurobiol. Exp (Wars). 69, 1-11.
26. Ikeda, K., Negishi, H., Yamori, Y., 2003. Antioxidant nutrients and hypoxia/ischemia brain injury in rodents. Toxicology 189, 55-61. (Pubitemid 36725022)
27. Johnston, K.C., Li, J.Y., Lyden, P.D., Hanson, S.K., Feasby, T.E., Adams, R.J., Faught Jr., R.E., Haley Jr., E.C., 1998. Medical and neurological complications of ischemic stroke: experience from the RANTTAS trial. RANTTAS Investigators. Stroke 29, 447-453. (Pubitemid 28086690)
28. Kielian, T., 2006. Toll-like receptors in central nervous system glial inflammation and homeostasis. J. Neurosci. Res. 83, 711-730.
29. Kim, J.W., Jin, Y.C., Kim, Y.M., Rhie, S., Kim, H.J., Seo, H.G., Lee, J.H., Ha, Y.L., Chang, K.C., 2009. Daidzein administration in vivo reduces myocardial injury in a rat ischemia/reperfusion model by inhibiting NF-kappaB activation. Life Sci. 84, 227-234.
30. Kumazawa, Y., Kawaguchi, K., Takimoto, H., 2006. Immunomodulating effects of flavonoids on acute and chronic inflammatory responses caused by tumor necrosis factor alpha. Curr. Pharm. Des. 12, 4271-4279. (Pubitemid 44669755)
31. Lawrence, T., Willoughby, D.A., Gilroy, D.W., 2002. Anti-inflammatory lipid mediators and insights into the resolution of inflammation. Nat. Rev. Immunol. 2, 787-795. (Pubitemid 37328718)
32. Lee, J.K., Kim, S.Y., Kim, Y.S., Lee, W.H., Hwang, D.H., Lee, J.Y., 2009. Suppression of the TRIF-dependent signaling pathway of Toll-like receptors by luteolin. Biochem. Pharmacol. 77, 1391-1400.
33. Longa, E.Z., Weinstein, P.R., Carlson, S., Cummins, R., 1989. Reversible middle cerebral artery occlusion without craniotomy in rats. Stroke 20, 84-91. (Pubitemid 19040218)
34. Maulik, N., Watanabe, M., Zu, Y.L., Huang, C.K., Cordis, G.A., Schley, J.A., Das, D.K., 1996. Ischemic preconditioning triggers the activation of MAP kinases and MAPKAP kinase 2 in rat hearts. FEBS Lett. 396, 233-237. (Pubitemid 26377830)
35. Nurmi, A., Lindsberg, P.J., Koistinaho, M., Zhang, W., Juettler, E., Karjalainen-Lindsberg, M.L., Weih, F., Frank, N., Schwaninger, M., Koistinaho, J., 2004. Nuclear factor-kappaB contributes to infarction after permanent focal ischemia. Stroke 35, 987-991. (Pubitemid 38419815)
36. Okun, E., Griffioen, K.J., Lathia, J.D., Tang, S.C., Mattson, M.P., Arumugam, T.V., 2009. Toll-like receptors in neurodegeneration. Brain Res. Rev. 59, 278-292.
37. Raingeaud, J., Gupta, S., Rogers, J.S., Dickens, M., Han, J., Ulevitch, R.J., Davis, R.J., 1995. Pro-inflammatory cytokines and environmental stress cause p38 mitogen-activated protein kinase activation by dual phosphorylation on tyrosine and threonine. J. Biol. Chem. 270, 7420-7426.
38. Safirstein, R., DiMari, J., Megyesi, J., Price, P., 1998. Mechanisms of renal repair and survival following acute injury. Semin. Nephrol. 18, 519-522. (Pubitemid 28430755)
39. Simonyi, A., Wang, Q., Miller, R.L., Yusof, M., Shelat, P.B., Sun, A.Y., Sun, G.Y., 2005. Polyphenols in cerebral ischemia: novel targets for neuroprotection. Mol. Neurobiol. 31, 135-147. (Pubitemid 41271199)
40. Sironi, L., Banfi, C., Brioschi, M., Gelosa, P., Guerrini, U., Nobili, E., Gianella, A., Paoletti, R., Tremoli, E., Cimino, M., 2006. Activation of NF-κB and ERK1/2 after permanent focal ischemia is abolished by simvastatin treatment. Neurobiol. Dis. 22, 445-451.
41. Soysa, N.S., Alles, N., 2009. NF-kappaB functions in osteoclasts. Biochem. Biophys. Res. Commun. 378, 1-5.
42. Tang, S.C., Arumugam, T.V., Xu, X., Cheng, A.,Mughal, M.R., Jo, D.G., Lathia, J.D., Siler, D.A., Chigurupati, S., Ouyang, X., Magnus, T., Camandola, S., Mattson, M.P., 2007. Pivotal role for neuronal Toll-like receptors in ischemic brain injury and functional deficits. Proc. Natl. Acad. Sci. U.S.A. 104, 13798-13803. (Pubitemid 350003400)
43. Tatlisumak, T., Carano, R.A., Takano, K., Opgenorth, T.J., Sotak, C.H., Fisher, M.A., 1998. Novel endothelin antagonist, A-127722, attenuates ischemic lesion size in rats with temporary middle cerebral artery occlusion: a diffusion and perfusion MRI study. Stroke 29, 850-857.
44. Theoharides, T.C., 2009. Luteolin as a therapeutic option for multiple sclerosis. J. Neuroinflammation 6, 29.
45. Thompson, W.L., Van Eldik, L.J., 2009. Inflammatory cytokines stimulate the chemokines CCL2/MCP-1 and CCL7/MCP-3 through NFkB and MAPK dependent pathways in rat astrocytes. Brain Res. 1287, 47-57.
46. Tsai, F.S., Peng, W.H., Wang, W.H., Wu, C.R., Hsieh, C.C., Lin, Y.T., Feng, I.C., Hsieh, M.T., 2007. Effects of luteolin on learning acquisition in rats: involvement of the central cholinergic system. Life Sci. 80, 1692-1698.
47. Van Zanden, J.J., Geraets, L., Wortelboer, H.M., van Bladeren, P.J., Rietjens, I.M., Cnubben, N.H., 2004. Structural requirements for the flavonoid-mediated modulation of glutathione S-transferase P1-1 and GS-X pump activity in MCF7 breast cancer cells. Biochem. Pharmacol. 67, 1607-1617. (Pubitemid 38388223)
48. Wang, L., Zhang, X., Liu, L., Cui, L., Yang, R., Li, M., Du, W., 2010. Tanshinone II A down-regulates HMGB1, RAGE, TLR4, NF-kappaB expression, ameliorates BBB permeability and endothelial cell function, and protects rat brains against focal ischemia. Brain Res. 1321, 143-151.
49. Wesche, H., Henzel, W.J., Shillinglaw, W., Li, S., Cao, Z., 1997. MyD88: an adapter that recruits IRAK to the IL-1 receptor complex. Immunity 7, 837-847. (Pubitemid 28064897)
50. Xia, Z., Dickens, M., Raingeaud, J., Davis, R.J., Greenberg, M.E., 1995. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270, 1326-1331.
51. Yang, C.H., Zhang, X.J., Fan, H.G., Liu, Y., 2009. Curcumin up-regulates transcription factor Nrf2, HO-1 expression and protects rat brains against focal ischemia. Brain Res. 1282, 133-141.
52. Yang, L., Tao, L.Y., Chen, X.P., 2007a. Roles of NF-kappaB in central nervous system damage and repair. Neurosci. Bull. 23, 307-313. (Pubitemid 350189506)
53. Yang, Y., Zhou, H., Yang, Y., Li, W., Zhou, M., Zeng, Z., Xiong, W., Wu, M., Huang, H., Zhou, Y., Peng, C., Huang, C., Li, X., Li, G., 2007b. Lipopolysaccharide (LPS) regulates TLR4 signal transduction in nasopharynx epithelial cell line 5-8F via NFkappaB and MAPKs signaling pathways. Mol. Immunol. 44, 984-992. (Pubitemid 44414996)
54. Yi, J.H., Park, S.W., Kapadia, R., Vemuganti, R., 2007. Role of transcription factors in mediating post-ischemic cerebral inflammation and brain damage. Neurochem. Int. 50, 1014-1027. (Pubitemid 46962819)
55. Youn, H.S., Lee, J.Y., Saitoh, S.I., Miyake, K., Kang, K.W., Choi, Y.J., Hwang, D.H., 2006. Suppression of MyD88- and TRIF-dependent signaling pathways of Toll-like receptor by (-)-epigallocatechin-3-gallate, a polyphenol component of green tea. Biochem. Pharmacol. 72, 850-859. (Pubitemid 44313886)
56. Zemke, D., Smith, J.L., Reeves, M.J., Majid, A., 2004. Ischemia and ischemic tolerance in the brain: an overview. Neurotoxicology 25, 895-904. (Pubitemid 39335582)
57. Zeng, H., Wu, H., Sloane, V., Jones, R., Yu, Y., Lin, P., Gewirtz, A.T., Neish, A.S., 2006. Flagellin/TLR5 responses in epithelia reveal intertwined activation of inflammatory and apoptotic pathways. Am. J. Physiol. Gastrointest. Liver Physiol. 290, 96-108.
58. Zhang, H.L., Gu, Z.L., Savitz, S.I., Han, F., Fukunaga, K., Qin, Z.H., 2008. Neuroprotective effects of prostaglandinA(1) in rat models of permanent focal cerebral ischemia are associated with nuclear factor-kappaB inhibition and peroxisome proliferator-activated receptor-gamma up-regulation. J. Neurosci. Res. 86, 1132-1141. (Pubitemid 351441311)
59. Zhao, G., Zang, S.Y., Jiang, Z.H., Chen, Y.Y., Ji, X.H., Lu, B.F.,Wu, J.H., Qin, G.W., Guo, L.H., 2011. Postischemic administration of liposome-encapsulated luteolin prevents against ischemia-reperfusion injury in a rat middle cerebral artery occlusion model. J. Nutr. Biochem. 22, 929-936.
60. Zheng, Z., Yenari, M.A., 2004. Post-ischemic inflammation: molecular mechanisms and therapeutic implications. Neurol. Res. 26, 884-992.