α-TLR2 antibody attenuates the Aβ-mediated inflammatory response in microglia through enhanced expression of SIGIRR

Brain, Behavior, and Immunity

Volumn 46, Issue , 2015, Pages 70-79

  Costello, Derek A ^a   Carney, Dónal G ^a   Lynch, Marina A ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Akt; A ; Hippocampus; LTP; Microglia; PI3 kinase; PPAR ; SIGIRR; TIR8; TLR2

Indexed keywords

2 CHLORO 5 NITROBENZANILIDE; 2 MORPHOLINO 8 PHENYLCHROMONE; ALPHA TOLL LIKE RECEPTOR 2 ANTIBODY; AMYLOID BETA PROTEIN; IMMUNOGLOBULIN G; INTERLEUKIN 6; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; RECEPTOR ANTIBODY; RECEPTOR PROTEIN; SINGLE IMMUNOGLOBULIN INTERLEUKIN 1 RELATED RECEPTOR; TOLL LIKE RECEPTOR 2; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; ANTIBODY; INTERLEUKIN 1 RECEPTOR; TIR8 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; INFLAMMATION; LONG TERM POTENTIATION; MALE; MICROGLIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR UPREGULATION; ANIMAL; GENETICS; HIPPOCAMPUS; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

AMYLOID BETA-PEPTIDES; ANIMALS; ANTIBODIES; HIPPOCAMPUS; INFLAMMATION; INTERLEUKIN-6; MICE; MICE, KNOCKOUT; MICROGLIA; RECEPTORS, INTERLEUKIN-1; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 2;

EID: 84928824107     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2015.01.005     Document Type: Article

References (56)

1. Adib-Conquy M., Adrie C., Fitting C., Gattolliat O., Beyaert R., Cavaillon J.M. Up-regulation of MyD88s and SIGIRR, molecules inhibiting Toll-like receptor signaling, in monocytes from septic patients. Crit. Care Med. 2006, 34:2377-2385.
2. Akiyama H., Barger S., Barnum S., Bradt B., Bauer J., Cole G.M., Cooper N.R., Eikelenboom P., Emmerling M., Fiebich B.L., Finch C.E., Frautschy S., Griffin W.S., Hampel H., Hull M., Landreth G., Lue L., Mrak R., Mackenzie I.R., McGeer P.L., O'Banion M.K., Pachter J., Pasinetti G., Plata-Salaman C., Rogers J., Rydel R., Shen Y., Streit W., Strohmeyer R., Tooyoma I., Van Muiswinkel F.L., Veerhuis R., Walker D., Webster S., Wegrzyniak B., Wenk G., Wyss-Coray T. Inflammation and Alzheimer's disease. Neurobiol. Aging 2000, 21:383-421.
3. Auvin S., Shin D., Mazarati A., Sankar R. Inflammation induced by LPS enhances epileptogenesis in immature rat and may be partially reversed by IL1RA. Epilepsia 2010, 51(suppl. 3):34-38.
4. Blok D.C., van Lieshout M.H., Hoogendijk A.J., Florquin S., de Boer O.J., Garlanda C., Mantovani A., van't Veer C., de Vos A.F., van der Poll T. Single immunoglobulin interleukin-1 receptor-related molecule impairs host defense during pneumonia and sepsis caused by Streptococcus pneumoniae. J. Innate Immunity 2014, 6:542-552.
5. Butovsky O., Jedrychowski M.P., Moore C.S., Cialic R., Lanser A.J., Gabriely G., Koeglsperger T., Dake B., Wu P.M., Doykan C.E., Fanek Z., Liu L., Chen Z., Rothstein J.D., Ransohoff R.M., Gygi S.P., Antel J.P., Weiner H.L. Identification of a unique TGF-beta-dependent molecular and functional signature in microglia. Nat. Neurosci. 2014, 17:131-143.
6. Camacho I.E., Serneels L., Spittaels K., Merchiers P., Dominguez D., De Strooper B. Peroxisome-proliferator-activated receptor gamma induces a clearance mechanism for the amyloid-beta peptide. J. Neurosci. 2004, 24:10908-10917.
7. Carpentier P.A., Duncan D.S., Miller S.D. Glial toll-like receptor signaling in central nervous system infection and autoimmunity. Brain Behav. Immun. 2008, 22:140-147.
8. Costello D.A., Herron C.E. The role of c-Jun N-terminal kinase in the A beta-mediated impairment of LTP and regulation of synaptic transmission in the hippocampus. Neuropharmacology 2004, 46:655-662.
9. Costello D.A., Lynch M.A. Toll-like receptor 3 activation modulates hippocampal network excitability, via glial production of interferon-beta. Hippocampus 2013, 23:696-707.
10. Costello D.A., O'Leary D.M., Herron C.E. Agonists of peroxisome proliferator-activated receptor-gamma attenuate the Abeta-mediated impairment of LTP in the hippocampus in vitro. Neuropharmacology 2005, 49:359-366.
11. Costello D.A., Lyons A., Denieffe S., Browne T.C., Cox F.F., Lynch M.A. Long term potentiation is impaired in membrane glycoprotein CD200-deficient mice: a role for Toll-like receptor activation. J. Biol. Chem. 2011, 286:34722-34732.
12. Costello D.A., Watson M.B., Cowley T.R., Murphy N., Murphy Royal C., Garlanda C., Lynch M.A. Interleukin-1alpha and HMGB1 mediate hippocampal dysfunction in SIGIRR-deficient mice. J. Neurosci. 2011, 31:3871-3879.
13. Davies J.M., MacSharry J., Shanahan F. Differential regulation of Toll-like receptor signalling in spleen and Peyer's patch dendritic cells. Immunology 2010, 131:438-448.
14. Gallagher J.J., Minogue A.M., Lynch M.A. Impaired performance of female APP/PS1 mice in the Morris water maze is coupled with increased Abeta accumulation and microglial activation. Neuro-degenerative diseases 2013, 11:33-41.
15. Garlanda C., Riva F., Polentarutti N., Buracchi C., Sironi M., De Bortoli M., Muzio M., Bergottini R., Scanziani E., Vecchi A., Hirsch E., Mantovani A. Intestinal inflammation in mice deficient in Tir8, an inhibitory member of the IL-1 receptor family. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:3522-3526.
16. Garlanda C., Riva F., Veliz T., Polentarutti N., Pasqualini F., Radaelli E., Sironi M., Nebuloni M., Zorini E.O., Scanziani E., Mantovani A. Increased susceptibility to colitis-associated cancer of mice lacking TIR8, an inhibitory member of the interleukin-1 receptor family. Canc. Res. 2007, 67:6017-6021.
17. Garlanda C., Anders H.J., Mantovani A. TIR8/SIGIRR: an IL-1R/TLR family member with regulatory functions in inflammation and T cell polarization. Trends Immunol. 2009, 30:439-446.
18. Gulen M.F., Kang Z., Bulek K., Youzhong W., Kim T.W., Chen Y., Altuntas C.Z., Sass Bak-Jensen K., McGeachy M.J., Do J.S., Xiao H., Delgoffe G.M., Min B., Powell J.D., Tuohy V.K., Cua D.J., Li X. The receptor SIGIRR suppresses Th17 cell proliferation via inhibition of the interleukin-1 receptor pathway and mTOR kinase activation. Immunity 2010, 32:54-66.
19. Hanke M.L., Kielian T. Toll-like receptors in health and disease in the brain: mechanisms and therapeutic potential. Clin. Sci. 2011, 121:367-387.
20. Hoffmann O., Braun J.S., Becker D., Halle A., Freyer D., Dagand E., Lehnardt S., Weber J.R. TLR2 mediates neuroinflammation and neuronal damage. J. Immunol. 2007, 178:6476-6481.
21. Huang X., Hazlett L.D., Du W., Barrett R.P. SIGIRR promotes resistance against Pseudomonas aeruginosa keratitis by down-regulating type-1 immunity and IL-1R1 and TLR4 signaling. J. Immunol. 2006, 177:548-556.
22. Jack C.S., Arbour N., Manusow J., Montgrain V., Blain M., McCrea E., Shapiro A., Antel J.P. TLR signaling tailors innate immune responses in human microglia and astrocytes. J. Immunol. 2005, 175:4320-4330.
23. Jana M., Palencia C.A., Pahan K. Fibrillar amyloid-beta peptides activate microglia via TLR2: implications for Alzheimer's disease. J. Immunol. 2008, 181:7254-7262.
24. Jiang X., McClellan S.A., Barrett R.P., Zhang Y., Hazlett L.D. Vasoactive intestinal peptide downregulates proinflammatory TLRs while upregulating anti-inflammatory TLRs in the infected cornea. J. Immunol. 2012, 189:269-278.
25. Kelly, R.J., Minogue, A.M., Lyons, A., Jones, R.S., Browne, T.C., Costello, D.A., Denieffe, S., O'Sullivan, C., Connor, T.J., Lynch, M.A., 2013. Glial Activation in AbetaPP/PS1 Mice is Associated with Infiltration of IFNgamma-Producing Cells. Journal of Alzheimer's disease: JAD.
26. 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.
27. Lech M., Garlanda C., Mantovani A., Kirschning C.J., Schlondorff D., Anders H.J. Different roles of TiR8/Sigirr on toll-like receptor signaling in intrarenal antigen-presenting cells and tubular epithelial cells. Kidney Int. 2007, 72:182-192.
28. Lech M., Kulkarni O.P., Pfeiffer S., Savarese E., Krug A., Garlanda C., Mantovani A., Anders H.J. Tir8/Sigirr prevents murine lupus by suppressing the immunostimulatory effects of lupus autoantigens. J. Exp. Med. 2008, 205:1879-1888.
29. 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.
30. Letiembre M., Liu Y., Walter S., Hao W., Pfander T., Wrede A., Schulz-Schaeffer W., Fassbender K. Screening of innate immune receptors in neurodegenerative diseases: a similar pattern. Neurobiol. Aging 2009, 30:759-768.
31. Liu S., Liu Y., Hao W., Wolf L., Kiliaan A.J., Penke B., Rube C.E., Walter J., Heneka M.T., Hartmann T., Menger M.D., Fassbender K. TLR2 is a primary receptor for Alzheimer's amyloid beta peptide to trigger neuroinflammatory activation. J. Immunol. 2012, 188:1098-1107.
32. Lynch M.A. The impact of neuroimmune changes on development of amyloid pathology; relevance to Alzheimer's disease. Immunology 2014, 141:292-301.
33. Lynch M.A. Neuroinflammatory changes negatively impact on LTP: a focus on IL-1beta. Brain Res. 2014.
34. Lyons A., Griffin R.J., Costelloe C.E., Clarke R.M., Lynch M.A. IL-4 attenuates the neuroinflammation induced by amyloid-beta in vivo and in vitro. J. Neurochem. 2007, 101:771-781.
35. Lyons A., Downer E.J., Costello D.A., Murphy N., Lynch M.A. Dok2 mediates the CD200Fc attenuation of Abeta-induced changes in glia. J. Neuroinflammation 2012, 9:107.
36. Maroso M., Balosso S., Ravizza T., Liu J., Aronica E., Iyer A.M., Rossetti C., Molteni M., Casalgrandi M., Manfredi A.A., Bianchi M.E., Vezzani A. Toll-like receptor 4 and high-mobility group box-1 are involved in ictogenesis and can be targeted to reduce seizures. Nat. Med. 2010, 16:413-419.
37. Mazarati A., Maroso M., Iori V., Vezzani A., Carli M. High-mobility group box-1 impairs memory in mice through both toll-like receptor 4 and receptor for advanced glycation end products. Exp. Neurol. 2011, 232:143-148.
38. Minogue A.M., Lynch A.M., Loane D.J., Herron C.E., Lynch M.A. Modulation of amyloid-beta-induced and age-associated changes in rat hippocampus by eicosapentaenoic acid. J. Neurochem. 2007, 103:914-926.
39. Minogue A.M., Barrett J.P., Lynch M.A. LPS-induced release of IL-6 from glia modulates production of IL-1beta in a JAK2-dependent manner. J. Neuroinflammation 2012, 9:126.
40. Nolan Y., Vereker E., Lynch A.M., Lynch M.A. Evidence that lipopolysaccharide-induced cell death is mediated by accumulation of reactive oxygen species and activation of p38 in rat cortex and hippocampus. Exp. Neurol. 2003, 184:794-804.
41. Nolan Y., Martin D., Campbell V.A., Lynch M.A. Evidence of a protective effect of phosphatidylserine-containing liposomes on lipopolysaccharide-induced impairment of long-term potentiation in the rat hippocampus. J. Neuroimmunol. 2004, 151:12-23.
42. Paintlia A.S., Paintlia M.K., Singh I., Singh A.K. IL-4-induced peroxisome proliferator-activated receptor gamma activation inhibits NF-kappaB trans activation in central nervous system (CNS) glial cells and protects oligodendrocyte progenitors under neuroinflammatory disease conditions: implication for CNS-demyelinating diseases. J. Immunol. 2006, 176:4385-4398.
43. Qin J., Qian Y., Yao J., Grace C., Li X. SIGIRR inhibits interleukin-1 receptor- and toll-like receptor 4-mediated signaling through different mechanisms. J. Biol. Chem. 2005, 280:25233-25241.
44. Reed-Geaghan E.G., Savage J.C., Hise A.G., Landreth G.E. CD14 and toll-like receptors 2 and 4 are required for fibrillar A{beta}-stimulated microglial activation. J. Neurosci. 2009, 29:11982-11992.
45. Riva F., Bonavita E., Barbati E., Muzio M., Mantovani A., Garlanda C. TIR8/SIGIRR is an interleukin-1 receptor/toll like receptor family member with regulatory functions in inflammation and immunity. Front. Immunol. 2012, 3:322.
46. Thomassen E., Renshaw B.R., Sims J.E. Identification and characterization of SIGIRR, a molecule representing a novel subtype of the IL-1R superfamily. Cytokine 1999, 11:389-399.
47. Uryu S., Harada J., Hisamoto M., Oda T. Troglitazone inhibits both post-glutamate neurotoxicity and low-potassium-induced apoptosis in cerebellar granule neurons. Brain Res. 2002, 924:229-236.
48. Veliz Rodriguez T., Moalli F., Polentarutti N., Paroni M., Bonavita E., Anselmo A., Nebuloni M., Mantero S., Jaillon S., Bragonzi A., Mantovani A., Riva F., Garlanda C. Role of toll interleukin-1 receptor (IL-1R) 8, a negative regulator of IL-1R/Toll-like receptor signaling, in resistance to acute Pseudomonas aeruginosa lung infection. Infect. Immunity 2012, 80:100-109.
49. Vereker E., Campbell V., Roche E., McEntee E., Lynch M.A. Lipopolysaccharide inhibits long term potentiation in the rat dentate gyrus by activating caspase-1. J. Biol. Chem. 2000, 275:26252-26258.
50. Vereker E., O'Donnell E., Lynch M.A. The inhibitory effect of interleukin-1beta on long-term potentiation is coupled with increased activity of stress-activated protein kinases. J. Neurosci. 2000, 20:6811-6819.
51. Villena J., Suzuki R., Fujie H., Chiba E., Takahashi T., Tomosada Y., Shimazu T., Aso H., Ohwada S., Suda Y., Ikegami S., Itoh H., Alvarez S., Saito T., Kitazawa H. Immunobiotic Lactobacillus jensenii modulates the toll-like receptor 4-induced inflammatory response via negative regulation in porcine antigen-presenting cells. Clin. Vaccine Immunol.: CVI 2012, 19:1038-1053.
52. Vollmar P., Kullmann J.S., Thilo B., Claussen M.C., Rothhammer V., Jacobi H., Sellner J., Nessler S., Korn T., Hemmer B. Active immunization with amyloid-beta 1-42 impairs memory performance through TLR2/4-dependent activation of the innate immune system. J. Immunol. 2010, 185:6338-6347.
53. Wald D., Qin J., Zhao Z., Qian Y., Naramura M., Tian L., Towne J., Sims J.E., Stark G.R., Li X. SIGIRR, a negative regulator of Toll-like receptor-interleukin 1 receptor signaling. Nat. Immunol. 2003, 4:920-927.
54. Watson M.B., Costello D.A., Carney D.G., McQuillan K., Lynch M.A. SIGIRR modulates the inflammatory response in the brain. Brain Behav. Immunity 2010, 24:985-995.
55. Wyss-Coray T. Inflammation in Alzheimer disease: driving force, bystander or beneficial response?. Nat. Med. 2006, 12:1005-1015.
56. Xing B., Xin T., Hunter R.L., Bing G. Pioglitazone inhibition of lipopolysaccharide-induced nitric oxide synthase is associated with altered activity of p38 MAP kinase and PI3K/Akt. J. Neuroinflammation 2008, 5:4.