Curcumin attenuates acute inflammatory injury by inhibiting the TLR4/MyD88/NF-κB signaling pathway in experimental traumatic brain injury

Journal of Neuroinflammation

Volumn 11, Issue , 2014, Pages

  Zhu, Hai tao ^a   Bian, Chen ^a   Yuan, Ji chao ^a   Chu, Wei hua ^a   Xiang, Xin ^a   Chen, Fei ^a   Wang, Cheng shi ^a   Feng, Hua ^a   Lin, Jiang kai ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Curcumin; Inflammation; Toll like receptor 4; Traumatic brain injury

Indexed keywords

CURCUMIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPOLYSACCHARIDE; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR 4;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTICLE; BRAIN CONTUSION; BRAIN EDEMA; BRAIN WATER; COCULTURE; CONTROLLED STUDY; CYTOKINE RELEASE; DRUG MECHANISM; EMBRYO; FEMALE; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE; MALE; MICROGLIA; MOUSE; NERVE CELL CULTURE; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRAUMATIC BRAIN INJURY; UPREGULATION;

ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; BRAIN EDEMA; BRAIN INJURIES; CELLS, CULTURED; CEREBRAL CORTEX; COCULTURE TECHNIQUES; CURCUMIN; DISEASE MODELS, ANIMAL; DOWN-REGULATION; EMBRYO, MAMMALIAN; ENCEPHALITIS; FEMALE; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MYELOID DIFFERENTIATION FACTOR 88; SIGNAL TRANSDUCTION; TIME FACTORS; TOLL-LIKE RECEPTOR 4;

EID: 84899574914     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-11-59     Document Type: Article

References (64)

1. Maas AI, Stocchetti N, Bullock R. Moderate and severe traumatic brain injury in adults. Lancet Neurol 2008, 7:728-741. 10.1016/S1474-4422(08)70164-9, 18635021.
2. Xiong Y, Mahmood A, Chopp M. Animal models of traumatic brain injury. Nat Rev Neurosci 2013, 14:128-142. 10.1038/nrn3407, 3951995, 23329160.
3. Helmy A, De Simoni MG, Guilfoyle MR, Carpenter KL, Hutchinson PJ. Cytokines and innate inflammation in the pathogenesis of human traumatic brain injury. ProgNeurobiol 2011, 95:352-372.
4. Ziebell JM, Morganti-Kossmann MC. Involvement of pro- and anti-inflammatory cytokines and chemokines in the pathophysiology of traumatic brain injury. Neurotherapeutics 2010, 7:22-30. 10.1016/j.nurt.2009.10.016, 20129494.
5. Takeuchi O, Akira S. Pattern recognition receptors and inflammation. Cell 2010, 140:805-820. 10.1016/j.cell.2010.01.022, 20303872.
6. Lin Q, Li M, Fang D, Fang J, Su SB. The essential roles of Toll-like receptor signaling pathways in sterile inflammatory diseases. Int Immunopharmacol 2011, 11:1422-1432. 10.1016/j.intimp.2011.04.026, 21600309.
7. Carpentier PA, Duncan DS, Miller SD. Glial toll-like receptor signaling in central nervous system infection and autoimmunity. Brain Behav Immun 2008, 22:140-147. 10.1016/j.bbi.2007.08.011, 2231624, 17920811.
8. Fang H, Wang PF, Zhou Y, Wang YC, Yang QW. Toll-like receptor 4 signaling in intracerebral hemorrhage-induced inflammation and injury. J Neuroinflammation 2013, 10:27. 10.1186/1742-2094-10-27, 3598479, 23414417.
9. Hyakkoku K, Hamanaka J, Tsuruma K, Shimazawa M, Tanaka H, Uematsu S, Akira S, Inagaki N, Nagai H, Hara H. Toll-like receptor 4 (Tlr4), but not Tlr3 or Tlr9, knock-out mice have neuroprotectiveeffects against focal cerebral ischemia. Neuroscience 2010, 171:258-267. 10.1016/j.neuroscience.2010.08.054, 20804821.
10. Ahmad A, Crupi R, Campolo M, Genovese T, Esposito E, Cuzzocrea S. Absence of TLR4 reduces neurovascular unit and secondary inflammatory process after traumatic brain injury in mice. PLoS One 2013, 8:e57208. 10.1371/journal.pone.0057208, 3610903, 23555560.
11. Li GZ, Zhang Y, Zhao JB, Wu GJ, Su XF, Hang CH. Expression of myeloid differentiation primary response protein 88 (Myd88) in the cerebral cortex after experimental traumatic brain injury in rats. Brain Res 2011, 1396:96-104.
12. Wang X, Stridh L, Li W, Dean J, Elmgren A, Gan L, Eriksson K, Hagberg H, Mallard C. Lipopolysaccharide sensitizes neonatal hypoxic-ischemic brain injury in a MyD88-dependent manner. J Immunol 2009, 183:7471-7477. 10.4049/jimmunol.0900762, 19917690.
13. Agarwal NB, Jain S, Agarwal NK, Mediratta PK, Sharma KK. Modulation of pentylenetetrazole-induced kindling and oxidative stress by curcumin in mice. Phytomedicine 2011, 18:756-759. 10.1016/j.phymed.2010.11.007, 21211953.
14. Yang F, Lim GP, Begum AN, Ubeda OJ, Simmons MR, Ambegaokar SS, Chen PP, Kayed R, Glabe CG, Frautschy SA, Cole GM. Curcumin inhibits formation of amyloid beta oligomers and fibrils, binds plaques, and reduces amyloid in vivo. J BiolChem 2005, 280:5892-5901.
15. Heger M, Van Golen RF, Broekgaarden M, Michel MC. The molecular basis for the pharmacokinetics and pharmacodynamics of curcumin and its metabolites in relation to cancer. Pharmacol Rev 2014, 66:222-307.
16. Sharma S, Ying Z, Gomez-Pinilla F. A pyrazolecurcumin derivative restores membrane homeostasis disrupted after brain trauma. Exp Neurol 2010, 226:191-199. 10.1016/j.expneurol.2010.08.027, 3225197, 20816821.
17. Laird MD, Sukumari-Ramesh S, Swift AE, Meiler SE, Vender JR, Dhandapani KM. Curcumin attenuates cerebral edema following traumatic brain injury in mice: a possible role for aquaporin-4?. J Neurochem 2010, 113:637-648. 10.1111/j.1471-4159.2010.06630.x, 2911034, 20132469.
18. Wu A, Ying Z, Schubert D, Gomez-Pinilla F. Brain and spinal cord interaction: a dietary curcumin derivative counteracts locomotor and cognitive deficits after brain trauma. Neurorehabil Neural Repair 2011, 25:332-342. 10.1177/1545968310397706, 3258099, 21343524.
19. Sharma S, Zhuang Y, Ying Z, Wu A, Gomez-Pinilla F. Dietary curcumin supplementation counteracts reduction in levels of molecules involved in energy homeostasis after brain trauma. Neuroscience 2009, 161:1037-1044. 10.1016/j.neuroscience.2009.04.042, 2805661, 19393301.
20. Youn HS, Saitoh SI, Miyake K, Hwang DH. Inhibition of homodimerization of Toll-like receptor 4 by curcumin. Biochem Pharmacol 2006, 72:62-69. 10.1016/j.bcp.2006.03.022, 16678799.
21. Zhao L, Lee JY, Hwang DH. Inhibition of pattern recognition receptor-mediated inflammation by bioactive phytochemicals. Nutr Rev 2011, 69:310-320. 10.1111/j.1753-4887.2011.00394.x, 3881972, 21631512.
22. Zeng Z, Zhan L, Liao H, Chen L, Lv X. Curcumin improves TNBS-induced colitis in rats by inhibiting IL-27 expression via the TLR4/NF-kappaB signaling pathway. Planta Med 2013, 79:102-109.
23. Tu CT, Han B, Yao QY, Zhang YA, Liu HC, Zhang SC. Curcumin attenuates Concanavalin A-induced liver injury in mice by inhibition of Toll-like receptor (TLR) 2, TLR4 and TLR9 expression. Int Immunopharmacol 2012, 12:151-157. 10.1016/j.intimp.2011.11.005, 22138522.
24. Meng Z, Yan C, Deng Q, Gao DF, Niu XL. Curcumin inhibits LPS-induced inflammation in rat vascular smooth muscle cells in vitro via ROS-relative TLR4-MAPK/NF-kappaB pathways. Acta Pharmacol Sin 2013, 34:901-911. 10.1038/aps.2013.24, 23645013.
25. Chearwae W, Bright JJ. 15-deoxy-Delta(12,14)-prostaglandin J(2) and curcumin modulate the expression of toll-like receptors 4 and 9 in autoimmune T lymphocyte. J Clin Immunol 2008, 28:558-570. 10.1007/s10875-008-9202-7, 18463970.
26. Feeney DM, Boyeson MG, Linn RT, Murray HM, Dail WG. Responses to cortical injury: I. Methodology and local effects of contusions in the rat. Brain Res 1981, 211:67-77. 10.1016/0006-8993(81)90067-6, 7225844.
27. Chen SF, Hsu CW, Huang WH, Wang JY. Post-injury baicalein improves histological and functional outcomes and reduces inflammatory cytokines after experimental traumatic brain injury. Br J Pharmacol 2008, 155:1279-1296. 10.1038/bjp.2008.345, 2607198, 18776918.
28. Roof RL, Duvdevani R, Heyburn JW, Stein DG. Progesterone rapidly decreases brain edema: treatment delayed up to 24 hours is still effective. Exp Neurol 1996, 138:246-251. 10.1006/exnr.1996.0063, 8620923.
29. Carlson NG, Rojas MA, Black JD, Redd JW, Hille J, Hill KE, Rose JW. Microglial inhibition of neuroprotection by antagonists of the EP1 prostaglandin E2 receptor. J Neuroinflammation 2009, 6:5. 10.1186/1742-2094-6-5, 2649915, 19222857.
30. Bian C, Zhu K, Yang L, Lin S, Li S, Su B, Zhang J. Gonadectomy differentially regulates steroid receptor coactivator-1 and synaptic proteins in the hippocampus of adult female and male C57BL/6 mice. Synapse 2012, 66:849-857. 10.1002/syn.21574, 22623226.
31. Schmued LC, Hopkins KJ. Fluoro-Jade B: a high affinity fluorescent marker for the localization of neuronal degeneration. Brain Res 2000, 874:123-130. 10.1016/S0006-8993(00)02513-0, 10960596.
32. Lee H, Lee S, Cho IH, Lee SJ. Toll-like receptors: sensor molecules for detecting damage to the nervous system. Curr Protein Pept Sci 2013, 14:33-42. 10.2174/1389203711314010006, 23441900.
33. Hanke ML, Kielian T. Toll-like receptors in health and disease in the brain: mechanisms and therapeutic potential. ClinSci (Lond) 2011, 121:367-387.
34. Lin S, Yin Q, Zhong Q, Lv FL, Zhou Y, Li JQ, Wang JZ, Su BY, Yang QW. Heme activates TLR4-mediated inflammatory injury via MyD88/TRIF signaling pathway in intracerebral hemorrhage. J Neuroinflammation 2012, 9:46. 10.1186/1742-2094-9-46, 3344687, 22394415.
35. Yang QW, Lu FL, Zhou Y, Wang L, Zhong Q, Lin S, Xiang J, Li JC, Fang CQ, Wang JZ. HMBG1 mediates ischemia-reperfusion injury by TRIF-adaptor independent Toll-like receptor 4 signaling. J Cereb Blood Flow Metab 2011, 31:593-605. 10.1038/jcbfm.2010.129, 3049514, 20700129.
36. Chen CC, Hung TH, Wang YH, Lin CW, Wang PY, Lee CY, Chen SF. Wogonin improves histological and functional outcomes, and reduces activation of TLR4/NF-kappaB signaling after experimental traumatic brain injury. PLoS One 2012, 7:e30294. 10.1371/journal.pone.0030294, 3260265, 22272328.
37. Helmy A, Carpenter KL, Menon DK, Pickard JD, Hutchinson PJ. The cytokine response to human traumatic brain injury: temporal profiles and evidence for cerebral parenchymal production. J Cereb Blood Flow Metab 2011, 31:658-670. 10.1038/jcbfm.2010.142, 3049520, 20717122.
38. Mao SS, Hua R, Zhao XP, Qin X, Sun ZQ, Zhang Y, Wu YQ, Jia MX, Cao JL, Zhang YM. Exogenous administration of PACAP alleviates traumatic brain injury in rats through a mechanism involving the TLR4/MyD88/NF-kappaB pathway. J Neurotrauma 1941-1959, 2012:29.
39. Chen G, Zhang S, Shi J, Ai J, Qi M, Hang C. Simvastatin reduces secondary brain injury caused by cortical contusion in rats: possible involvement of TLR4/NF-kappaB pathway. Exp Neurol 2009, 216:398-406. 10.1016/j.expneurol.2008.12.019, 19166837.
40. Anand P, Kunnumakkara AB, Newman RA, Aggarwal BB. Bioavailability of curcumin: problems and promises. Mol Pharm 2007, 4:807-818. 10.1021/mp700113r, 17999464.
41. Pan MH, Huang TM, Lin JK. Biotransformation of curcumin through reduction and glucuronidation in mice. Drug Metab Dispos 1999, 27:486-494.
42. Ravindranath V, Chandrasekhara N. Absorption and tissue distribution of curcumin in rats. Toxicology 1980, 16:259-265. 10.1016/0300-483X(80)90122-5, 7423534.
43. Shoba G, Joy D, Joseph T, Majeed M, Rajendran R, Srinivas PS. Influence of piperine on the pharmacokinetics of curcumin in animals and human volunteers. Planta Med 1998, 64:353-356. 10.1055/s-2006-957450, 9619120.
44. Wu A, Ying Z, Gomez-Pinilla F. Dietary curcumin counteracts the outcome of traumatic brain injury on oxidative stress, synaptic plasticity, and cognition. Exp Neurol 2006, 197:309-317. 10.1016/j.expneurol.2005.09.004, 16364299.
45. King MD, McCracken DJ, Wade FM, Meiler SE, Alleyne CH, Dhandapani KM. Attenuation of hematoma size and neurological injury with curcumin following intracerebral hemorrhage in mice. J Neurosurg 2011, 115:116-123. 10.3171/2011.2.JNS10784, 3153730, 21417704.
46. Covert MW, Leung TH, Gaston JE, Baltimore D. Achieving stability of lipopolysaccharide-induced NF-kappaB activation. Science 1854-1857, 2005:309.
47. Lumpkins K, Bochicchio GV, Zagol B, Ulloa K, Simard JM, Schaub S, Meyer W, Scalea T. Plasma levels of the beta chemokine regulated upon activation, normal T cell expressed, and secreted (RANTES) correlate with severe brain injury. J Trauma 2008, 64:358-361. 10.1097/TA.0b013e318160df9b, 18301198.
48. Lubbad A, Oriowo MA, Khan I. Curcumin attenuates inflammation through inhibition of TLR-4 receptor in experimental colitis. Mol Cell Biochem 2009, 322:127-135. 10.1007/s11010-008-9949-4, 19002562.
49. Tu CT, Yao QY, Xu BL, Wang JY, Zhou CH, Zhang SC. Protective effects of curcumin against hepatic fibrosis induced by carbon tetrachloride: modulation of high-mobility group box 1, Toll-like receptor 4 and 2 expression. Food ChemToxicol 2012, 50:3343-3351.
50. Liu K, Shen L, Wang J, Dong G, Wu H, Shao H, Jing H. The preventative role of curcumin on the lung inflammatory response induced by cardiopulmonary bypass in rats. J Surg Res 2012, 174:73-82. 10.1016/j.jss.2010.12.002, 21324484.
51. Buchanan MM, Hutchinson M, Watkins LR, Yin H. Toll-like receptor 4 in CNS pathologies. J Neurochem 2010, 114:13-27. 2909662, 20402965.
52. Barton GM, Medzhitov R. Toll-like receptor signaling pathways. Science 2003, 300:1524-1525. 10.1126/science.1085536, 12791976.
53. Rivest S. Regulation of innate immune responses in the brain. Nat Rev Immunol 2009, 9:429-439. 10.1038/nri2565, 19461673.
54. Walker PA, Shah SK, Jimenez F, Aroom KR, Harting MT, Cox CS. Bone marrow-derived stromal cell therapy for traumatic brain injury is neuroprotective via stimulation of non-neurologic organ systems. Surgery 2012, 152:790-793. 10.1016/j.surg.2012.06.006, 22853856.
55. Zujovic V, Taupin V. Use of cocultured cell systems to elucidate chemokine-dependent neuronal/microglial interactions: control of microglial activation. Methods 2003, 29:345-350. 10.1016/S1046-2023(02)00358-4, 12725801.
56. Yang S, Zhang D, Yang Z, Hu X, Qian S, Liu J, Wilson B, Block M, Hong JS. Curcumin protects dopaminergic neuron against LPS induced neurotoxicity in primary rat neuron/glia culture. Neurochem Res 2044-2053, 2008:33.
57. Karlstetter M, Lippe E, Walczak Y, Moehle C, Aslanidis A, Mirza M, Langmann T. Curcumin is a potent modulator of microglial gene expression and migration. J Neuroinflammation 2011, 8:125. 10.1186/1742-2094-8-125, 3192695, 21958395.
58. Lehnardt S. Innate immunity and neuroinflammation in the CNS: the role of microglia in Toll-like receptor-mediated neuronal injury. Glia 2010, 58:253-263.
59. Yao L, Kan EM, Lu J, Hao A, Dheen ST, Kaur C, Ling EA. Toll-like receptor 4 mediates microglial activation and production of inflammatory mediators in neonatal rat brain following hypoxia: role of TLR4 in hypoxic microglia. J Neuroinflammation 2013, 10:23. 10.1186/1742-2094-10-23, 3575244, 23388509.
60. Lehnardt S, Schott E, Trimbuch T, Laubisch D, Krueger C, Wulczyn G, Nitsch R, Weber JR. A vicious cycle involving release of heat shock protein 60 from injured cells and activation of toll-like receptor 4 mediates neurodegeneration in the CNS. J Neurosci 2008, 28:2320-2331. 10.1523/JNEUROSCI.4760-07.2008, 18322079.
61. Vartanian KB, Stevens SL, Marsh BJ, Williams-Karnesky R, Lessov NS, Stenzel-Poore MP. LPS preconditioning redirects TLR signaling following stroke: TRIF-IRF3 plays a seminal role in mediating tolerance to ischemic injury. J Neuroinflammation 2011, 8:140. 10.1186/1742-2094-8-140, 3217906, 21999375.
62. Marsh B, Stevens SL, Packard AE, Gopalan B, Hunter B, Leung PY, Harrington CA, Stenzel-Poore MP. Systemic lipopolysaccharide protects the brain from ischemic injury by reprogramming the response of the brain to stroke: a critical role for IRF3. J Neurosci 2009, 29:9839-9849. 10.1523/JNEUROSCI.2496-09.2009, 2946887, 19657036.
63. Longhi L, Gesuete R, Perego C, Ortolano F, Sacchi N, Villa P, Stocchetti N, De Simoni MG. Long-lasting protection in brain trauma by endotoxin preconditioning. J Cereb Blood Flow Metab 1919-1929, 2011:31.
64. Chen Z, Jalabi W, Shpargel KB, Farabaugh KT, Dutta R, Yin X, Kidd GJ, Bergmann CC, Stohlman SA, Trapp BD. Lipopolysaccharide-induced microglial activation and neuroprotection against experimental brain injury is independent of hematogenous TLR4. J Neurosci 2012, 32:11706-11715. 10.1523/JNEUROSCI.0730-12.2012, 22915113.