Toll-like 4 receptor inhibitor TAK-242 decreases neuroinflammation in rat brain frontal cortex after stress

Journal of Neuroinflammation

Volumn 11, Issue , 2014, Pages

  Gárate, Iciar ^a,b   García Bueno, Borja ^a,b   Madrigal, José Luis M ^a,b   Caso, Javier R ^a,b   Alou, Luis ^a   Gómez Lus, María L ^a   Leza, Juan C ^a,b  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED DE SALUD MENTAL CIBERSAM   (Spain)

Author keywords

Bacterial translocation; Frontal cortex; Neuroinflammation; Restraint stress; TLR 4 signalling

Indexed keywords

ANTIBIOTIC AGENT; BACTERIUM LIPOPOLYSACCHARIDE; MESSENGER RNA; PENICILLIN G; RESATORVID; STREPTOMYCIN SULFATE; TOLL LIKE RECEPTOR 4;

ACUTE STRESS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; BACTERIAL TRANSLOCATION; CONTROLLED STUDY; FRONTAL CORTEX; GRAM NEGATIVE BACTERIUM; IMMOBILIZATION STRESS; INTESTINE FLORA; INTESTINE MUCOSA PERMEABILITY; MALE; NERVOUS SYSTEM INFLAMMATION; NEUROMODULATION; NEUROPROTECTION; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; RAT; RECEPTOR UPREGULATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALS; BACTERIAL TRANSLOCATION; CYCLOOXYGENASE 2; ENCEPHALITIS; FRONTAL LOBE; IMMUNITY, INNATE; INTESTINES; LIPID PEROXIDATION; LIPOPOLYSACCHARIDES; MALE; NF-KAPPA B; NITRIC OXIDE SYNTHASE TYPE II; RATS; SIGNAL TRANSDUCTION; STRESS, PSYCHOLOGICAL; SULFONAMIDES; TOLL-LIKE RECEPTOR 4; TUBULIN;

EID: 84892386793     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-11-8     Document Type: Article

References (61)

1. Akira S, Takeda K. Toll-like receptor signalling. Nat Rev Immunol 2004, 4:499-511. 10.1038/nri1391, 15229469.
2. Finsen B, Owens T. Innate immune responses in central nervous system inflammation. FEBS Lett 2011, 585:3806-3812. 10.1016/j.febslet.2011.05.030, 21624366.
3. Hanisch UK, Johnson TV, Kipnis J. Toll-like receptors: roles in neuroprotection?. Trends Neurosci 2008, 31:176-182. 10.1016/j.tins.2008.01.005, 18329736.
4. Medzhitov R. Toll-like receptors and innate immunity. Nat Rev Immunol 2011, 1:135-145.
5. Lucas K, Maes M. Role of the toll like receptor (TLR) radical cycle in chronic inflammation: possible treatments targeting the TLR4 pathway. Mol Neurobiol 2013, 48:190-204. 10.1007/s12035-013-8425-7, 23436141.
6. Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell 2006, 124:783-801. 10.1016/j.cell.2006.02.015, 16497588.
7. Hanke ML, Kielian T. Toll-like receptors in health and disease in the brain: mechanisms and therapeutic potential. Clin Sci (Lond) 2011, 121:367-387. 10.1042/CS20110164, 21745188.
8. Piccinini AM, Midwood KS. DAMPening inflammation by modulating TLR signalling. Mediators Inflamm Epub 2010 Jul 13. Mediators Inflamm. 2010;2010. doi: 10.1155/2010/672395. Epub 2010 Jul 13.
9. Fischer M, Ehlers M. Toll-like receptors in autoimmunity. Ann N Y Acad Sci 2008, 1143:21-34. 10.1196/annals.1443.012, 19076342.
10. Kigerl KA, Popovich PG. Toll-like receptors in spinal cord injury. Curr Top Microbiol Immunol 2009, 336:121-136.
11. Takeuchi O, Akira S. Toll-like receptors; their physiological role and signal transduction system. Int Immunopharmacol 2001, 1:625-635. 10.1016/S1567-5769(01)00010-8, 11357875.
12. Shimazu R, Akashi S, Ogata H, Nagai Y, Fukudome K, Miyake K, Kimoto M, et al. MD-2, a molecule that confers lipopolysaccharide responsiveness on toll-like receptor 4. J Exp Med 1999, 189:1777-1782. 10.1084/jem.189.11.1777, 2193086, 10359581.
13. Means TK, Golenbock DT, Fenton MJ. The biology of toll-like receptors. Cytokine Growth Factor Rev 2000, 11:219-232. 10.1016/S1359-6101(00)00006-X, 10817965.
14. Madrigal JL, García-Bueno B, Caso JR, Pérez-Nievas BG, Leza JC, et al. Stress-induced oxidative changes in brain. CNS Neurol Disord Drug Targets 2006, 5:561-568. 10.2174/187152706778559327, 17073658.
15. Raison CL, Capuron L, Miller AH. Cytokines sing the blues: inflammation and the pathogenesis of depression. Trends Immunol 2006, 27:24-31. 10.1016/j.it.2005.11.006, 3392963, 16316783.
16. Maes M, Coucke F, Leunis JC. Normalization of the increased translocation of endotoxin from gram negative enterobacteria (leaky gut) is accompanied by a remission of chronic fatigue syndrome. Neuro Endocrinol Lett 2007, 28:739-744.
17. Herbert TB, Cohen S. Stress and immunity in humans: a meta-analytic review. Psychosom Med 1993, 55:364-379.
18. García-Bueno B, Caso JR, Leza JC. Stress as a neuroinflammatory condition in brain: damaging and protective mechanisms. Neurosci Biobehav Rev 2008, 32:1136-1151. 10.1016/j.neubiorev.2008.04.001, 18468686.
19. Buchanan MM, Hutchinson M, Watkins LR, Yin H. Toll-like receptor 4 in CNS pathologies. J Neurochem 2010, 114:13-27. 2909662, 20402965.
20. Ponferrada A, Caso JR, Alou L, Colón A, Sevillano D, Moro MA, Lizasoain I, Menchén P, Gómez-Lus ML, Lorenzo P, Cos E, Leza JC, Menchén L, et al. The role of PPARgamma on restoration of colonic homeostasis after experimental stress-induced inflammation and dysfunction. Gastroenterology 2007, 132:1791-1803. 10.1053/j.gastro.2007.02.032, 17484875.
21. Maes M, Kubera M, Leunis JC. The gut-brain barrier in major depression: intestinal mucosal dysfunction with an increased translocation of LPS from gram negative enterobacteria (leaky gut) plays a role in the inflammatory pathophysiology of depression. Neuro Endocrinol Lett 2008, 29:117-124.
22. Zacharowski K, Zacharowski PA, Koch A, Baban A, Tran N, Berkels R, Papewalis C, Schulze-Osthoff K, Knuefermann P, Zähringer U, Schumann RR, Rettori V, McCann SM, Bornstein SR, et al. Toll-like receptor 4 plays a crucial role in the immune-adrenal response to systemic inflammatory response syndrome. Proc Natl Acad Sci U S A 2006, 103:6392-6397. 10.1073/pnas.0601527103, 1458888, 16606831.
23. Caso JR, Pradillo JM, Hurtado O, Leza JC, Moro MA, Lizasoain I, et al. Toll-like receptor 4 is involved in subacute stress-induced neuroinflammation and in the worsening of experimental stroke. Stroke 2008, 39:1314-1320. 10.1161/STROKEAHA.107.498212, 18309167.
24. Gárate I, García-Bueno B, Madrigal JL, Bravo L, Berrocoso E, Caso JR, Micó JA, Leza JC, et al. Origin and consequences of brain toll-like receptor 4 pathway stimulation in an experimental model of depression. J Neuroinflammation 2011, 8:151. 10.1186/1742-2094-8-151, 3219571, 22053929.
25. Li M, Matsunaga N, Hazeki K, Nakamura K, Takashima K, Seya T, Hazeki O, Kitazaki T, Iizawa Y, et al. A novel cyclohexene derivative, ethyl (6R)-6-[N-(2-Chloro-4-fluorophenyl)sulfamoyl]cyclohex-1-ene-1-carboxylate (TAK-242), selectively inhibits toll-like receptor 4-mediated cytokine production through suppression of intracellular signaling. Mol Pharmacol 2006, 69:1288-1295. 10.1124/mol.105.019695, 16373689.
26. Takashima K, Matsunaga N, Yoshimatsu M, Hazeki K, Kaisho T, Uekata M, Hazeki O, Akira S, Iizawa Y, Ii M, et al. Analysis of binding site for the novel small-molecule TLR4 signal transduction inhibitor TAK-242 and its therapeutic effect on mouse sepsis model. Br J Pharmacol 2009, 157:1250-1262. 10.1111/j.1476-5381.2009.00297.x, 2743844, 19563534.
27. Kawamoto T, Ii M, Kitazaki T, Iizawa Y, Kimura H, et al. TAK-242 selectively suppresses toll-like receptor 4-signaling mediated by the intracellular domain. Eur J Pharmacol 2008, 584:40-48. 10.1016/j.ejphar.2008.01.026, 18299127.
28. Matsunaga N, Tsuchimori N, Matsumoto T, Ii M, et al. TAK-242 (resatorvid), a small-molecule inhibitor of Toll-like receptor (TLR) 4 signaling, binds selectively to TLR4 and interferes with interactions between TLR4 and its adaptor molecules. Mol Pharmacol 2011, 79:34-41. 10.1124/mol.110.068064, 20881006.
29. Yao L, Kan EM, Lu J, Hao A, Dheen ST, Kaur C, Ling EA, et al. 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.
30. Ando T, Brown RF, Berg RD, Dunn AJ, et al. Bacterial translocation can increase plasma corticosterone and brain catecholamine and indoleamine metabolism. Am J Physiol Regul Integr Comp Physiol 2000, 279:R2164-R2172.
31. Leza JC, Salas E, Sawicki G, Russell JC, Radomski MW, et al. The effects of stress on homeostasis in JCR-LA-cp rats: the role of nitric oxide. J Pharmacol Exp Ther 1998, 286:1397-1403.
32. Radley JJ, Arias CM, Sawchenko PE. Regional differentiation of the medial prefrontal cortex in regulating adaptive responses to acute emotional stress. J Neurosci 2006, 26:12967-12976. 10.1523/JNEUROSCI.4297-06.2006, 17167086.
33. Schreiber E, Matthias P, Muller MM, Schaffner W, et al. Rapid detection of octamer binding proteins with ';mini-extracts', prepared from a small number of cells. Nucleic Acids Res 1989, 17:6419. 10.1093/nar/17.15.6419, 318318, 2771659.
34. Li XH, Gong JP, Tu B, Shi YJ, Liu CA, et al. In vivo expression of lipopolysaccharide binding protein and its gene induced by endotoxin. Chin J Traumatol 2003, 6:280-283.
35. Das NP, Ratty AK. Studies on the effects of the narcotic alkaloids, cocaine, morphine and codeine on nonenzymatic lipid peroxidation in rat brain mitochondria. Biochem Med Metab Biol 1987, 37:256-264.
36. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254. 10.1016/0003-2697(76)90527-3, 942051.
37. Gárate I, Garcia-Bueno B, Madrigal JL, Caso JR, Alou L, Gomez-Lus ML, Micó JA, Leza JC, et al. Stress-induced neuroinflammation: role of the toll-like receptor-4 pathway. Biol Psychiatry 2013, 73:32-43. 10.1016/j.biopsych.2012.07.005, 22906518.
38. Fukata M, Michelsen KS, Eri R, Thomas LS, Hu B, Lukasek K, Nast CC, Lechago J, Xu R, Naiki Y, Soliman A, Arditi M, Abreu MT, et al. Toll-like receptor-4 is required for intestinal response to epithelial injury and limiting bacterial translocation in a murine model of acute colitis. Am J Physiol Gastrointest Liver Physiol 2005, 288:G1055-G1065. 10.1152/ajpgi.00328.2004, 15826931.
39. Poltorak A, He X, Smirnova I, Liu MY, Van Huffel C, Du X, Birdwell D, Alejos E, Silva M, Galanos C, Freudenberg M, Ricciardi-Castagnoli P, Layton B, Beutler B, et al. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 1998, 282:2085-2088.
40. Makkouk A, Abdelnoor AM. The potential use of Toll-like receptor (TLR) agonists and antagonists as prophylactic and/or therapeutic agents. Immunopharmacol Immunotoxicol 2009, 31:331-338. 10.1080/08923970902802926, 19555209.
41. Tsan MF, Gao B. Endogenous ligands of toll-like receptors. J Leukoc Biol 2004, 76:514-519. 10.1189/jlb.0304127, 15178705.
42. Fleshner M. Stress-evoked sterile inflammation, danger associated molecular patterns (DAMPs), microbial associated molecular patterns (MAMPs) and the inflammasome. Brain Behav Immun 2013, 27:1-7.
43. Moghaddam B. Stress preferentially increases extraneuronal levels of excitatory amino acids in the prefrontal cortex: comparison to hippocampus and basal ganglia. J Neurochem 1993, 60:1650-1657. 10.1111/j.1471-4159.1993.tb13387.x, 8097232.
44. Glezer I, Zekki H, Scavone C, Rivest S, et al. Modulation of the innate immune response by NMDA receptors has neuropathological consequences. J Neurosci 2003, 23:11094-11103.
45. Kizaki T, Izawa T, Sakurai T, Haga S, Taniguchi N, Tajiri H, Watanabe K, Day NK, Toba K, Ohno H, et al. Beta2-adrenergic receptor regulates toll-like receptor-4-induced nuclear factor-kappaB activation through beta-arrestin 2. Immunology 2008, 124:348-356. 10.1111/j.1365-2567.2007.02781.x, 2440829, 18194271.
46. Chaniotou Z, Giannogonas P, Theoharis S, Teli T, Gay J, Savidge T, Koutmani Y, Brugni J, Kokkotou E, Pothoulakis C, Karalis KP, et al. Corticotropin-releasing factor regulates TLR4 expression in the colon and protects mice from colitis. Gastroenterology 2010, 139:2083-2092. 10.1053/j.gastro.2010.08.024, 20732324.
47. Laflamme N, Rivest S. Toll-like receptor 4: the missing link of the cerebral innate immune response triggered by circulating gram-negative bacterial cell wall components. FASEB J 2001, 15:155-163. 10.1096/fj.00-0339com, 11149903.
48. Lehnardt S, Lachance C, Patrizi S, Lefebvre S, Follett PL, Jensen FE, Rosenberg PA, Volpe JJ, Vartanian T, et al. The toll-like receptor TLR4 is necessary for lipopolysaccharide-induced oligodendrocyte injury in the CNS. J Neurosci 2002, 22:2478-2486.
49. Zhang Y, Woodruff M, Zhang Y, Miao J, Hanley G, Stuart C, Zeng X, Prabhakar S, Moorman J, Zhao B, Yin D, et al. Toll-like receptor 4 mediates chronic restraint stress-induced immune suppression. J Neuroimmunol 2008, 194:115-122. 10.1016/j.jneuroim.2007.12.002, 2680718, 18192029.
50. Wang RP, Yao Q, Xiao YB, Zhu SB, Yang L, Feng JM, Li DZ, Li XL, Wu JJ, Chen J, et al. Toll-like receptor 4/nuclear factor-kappa B pathway is involved in myocardial injury in a rat chronic stress model. Stress 2011, 14:567-575. 10.3109/10253890.2011.571729, 21675862.
51. Tang SC, Arumugam TV, Xu X, Cheng A, Mughal MR, Jo DG, Lathia JD, Siler DA, Chigurupati S, Ouyang X, Magnus T, Camandola S, Mattson MP, et al. Pivotal role for neuronal toll-like receptors in ischemic brain injury and functional deficits. Proc Natl Acad Sci U S A 2007, 104:13798-13803. 10.1073/pnas.0702553104, 1959462, 17693552.
52. Okun E, Barak B, Saada-Madar R, Rothman SM, Griffioen KJ, Roberts N, Castro K, Mughal MR, Pita MA, Stranahan AM, Arumugam TV, Mattson MP, et al. Evidence for a developmental role for TLR4 in learning and memory. PLoS One 2012, 7:e47522. 10.1371/journal.pone.0047522, 3469493, 23071817.
53. Olson JK, Miller SD. Microglia initiate central nervous system innate and adaptive immune responses through multiple TLRs. J Immunol 2004, 173:3916-3924.
54. Kilic U, Kilic E, Matter CM, Bassetti CL, Hermann DM, et al. TLR-4 deficiency protects against focal cerebral ischemia and axotomy-induced neurodegeneration. Neurobiol Dis 2008, 31:33-40. 10.1016/j.nbd.2008.03.002, 18486483.
55. Sha T, Sunamoto M, Kitazaki T, Sato J, Ii M, Iizawa Y, et al. Therapeutic effects of TAK-242, a novel selective toll-like receptor 4 signal transduction inhibitor, in mouse endotoxin shock model. Eur J Pharmacol 2007, 571:231-239. 10.1016/j.ejphar.2007.06.027, 17632100.
56. Sha T, Iizawa Y, Ii M. Combination of imipenem and TAK-242, a toll-like receptor 4 signal transduction inhibitor, improves survival in a murine model of polymicrobial sepsis. Shock 2011, 35:205-209. 10.1097/SHK.0b013e3181f48942, 20720515.
57. Wittebole X, Castanares-Zapatero D, Laterre PF. Toll-like receptor 4 modulation as a strategy to treat sepsis. Mediators Inflamm 2010, 568396.
58. Rice TW, Wheeler AP, Bernard GR, Vincent JL, Angus DC, Aikawa N, Demeyer I, Sainati S, Amlot N, Cao C, Ii M, Matsuda H, Mouri K, Cohen J, et al. A randomized, double-blind, placebo-controlled trial of TAK-242 for the treatment of severe sepsis. Crit Care Med 2010, 38:1685-1694. 10.1097/CCM.0b013e3181e7c5c9, 20562702.
59. Griffiths MR, Gasque P, Neal JW. The regulation of the CNS innate immune response is vital for the restoration of tissue homeostasis (repair) after acute brain injury: a brief review. Int J Inflam 2010, 151097. This is all the information I have got Int J Inflam. 2010 Aug 9;2010:151097. doi:10.4061/2010/151097.
60. Kigerl KA, Lai W, Rivest S, Hart RP, Satoskar AR, Popovich PG, et al. Toll-like receptor (TLR)-2 and TLR-4 regulate inflammation, gliosis, and myelin sparing after spinal cord injury. J Neurochem 2007, 102:37-50. 10.1111/j.1471-4159.2007.04524.x, 17403033.
61. Romanovsky AA, Steiner AA, Matsumura K. Cells that trigger fever. Cell Cycle 2006, 5:2195-2197. 10.4161/cc.5.19.3321, 16969135.