Suppression of Alzheimer-associated inflammation by microglial prostaglandin-E2 EP4 receptor signaling

Journal of Neuroscience

Volumn 34, Issue 17, 2014, Pages 5882-5894

  Woodling, Nathaniel S ^a,b,d   Wang, Qian ^a   Priyam, Prachi G ^a   Larkin, Paul ^a   Shi, Ju ^a   Johansson, Jenny U ^a   Zagol Ikapitte, Irene ^c   Boutaud, Olivier ^c   Andreasson, Katrin I ^a,b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b STANFORD UNIVERSITY   (United States)

^c VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Alzheimer's disease; Microglia; Neuroinflammation; Peptide; Receptor

Indexed keywords

ALDEHYDE; AMYLOID BETA PROTEIN [1-40]; AMYLOID BETA PROTEIN [1-42]; CD11B ANTIGEN; CYCLOOXYGENASE 2; FLUORESCEIN ISOTHIOCYANATE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERFERON REGULATORY FACTOR 1; INTERFERON REGULATORY FACTOR 7; INTERLEUKIN 12P40; INTERLEUKIN 1BETA; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MESSENGER RNA; NUCLEAR RECEPTOR NUR77; NUCLEAR RECEPTOR RELATED FACTOR 1; POSTSYNAPTIC DENSITY PROTEIN 95; PROSTAGLANDIN E RECEPTOR 3; PROSTAGLANDIN E RECEPTOR 4; PROSTAGLANDIN E2; PROSTAGLANDIN RECEPTOR STIMULATING AGENT; STAT PROTEIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

AGED; ALZHEIMER DISEASE; AMYLOID PLAQUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BRAIN CORTEX; BRAIN TISSUE; CELL VIABILITY; CONTROLLED STUDY; ELECTROSPRAY MASS SPECTROMETRY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE DELETION; GENE EXPRESSION; HUMAN; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; LIQUID CHROMATOGRAPHY; MALE; MICROARRAY ANALYSIS; MICROGLIA; MOUSE; NERVE DEGENERATION; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN MODIFICATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UNINDEXED SEQUENCE; VERY ELDERLY; WESTERN BLOTTING;

ALZHEIMER'S DISEASE; AΒ PEPTIDE; MICROGLIA; NEUROINFLAMMATION; PGE2; RECEPTOR;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; CELL SURVIVAL; HUMANS; INFLAMMATION; METHYL ETHERS; MICROGLIA; PEPTIDE FRAGMENTS; RECEPTORS, PROSTAGLANDIN E, EP4 SUBTYPE; SIGNAL TRANSDUCTION;

EID: 84899490472     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0410-14.2014     Document Type: Article

References (51)

1. Akiyama H, Barger S, Barnum S, Bradt B, Bauer J, Cole GM, Cooper NR, Eikelenboom P, Emmerling M, Fiebich BL, Finch CE, Frautschy S, Griffin WS, Hampel H, Hull M, Landreth G, Lue L, Mrak R, Mackenzie IR, McGeer PL, et al. (2000) Inflammation and Alzheimer's disease. Neurobiol Aging 21:383-421. CrossRef Medline
2. 2 inhibits alveolar macrophage phagocytosis through an E-prostanoid 2 receptormediated increase in intracellular cyclic AMP. J Immunol 173:559-565. Medline
3. Boillée S, Yamanaka K, Lobsiger CS, Copeland NG, Jenkins NA, Kassiotis G, Kollias G, Cleveland DW (2006) Onset and progression in inherited ALS determined by motor neurons and microglia. Science 312:1389-1392. CrossRef Medline
4. Boutaud O, Montine TJ, Chang L, Klein WL, Oates JA (2006) PGH2-derived levuglandin adducts increase the neurotoxicity of amyloid beta1-42. J Neurochem 96:917-923. CrossRef Medline
5. Breitner JC, Baker LD, Montine TJ, Meinert CL, Lyketsos CG, Ashe KH, Brandt J, Craft S, Evans DE, Green RC, Ismail MS, Martin BK, Mullan MJ, Sabbagh M, Tariot PN (2011) Extended results of the Alzheimer's disease anti-inflammatory prevention trial. Alzheimers Dement 7:402-411. CrossRef Medline
6. Cardona AE, Pioro EP, Sasse ME, Kostenko V, Cardona SM, Dijkstra IM, Huang D, Kidd G, Dombrowski S, Dutta R, Lee JC, Cook DN, Jung S, Lira SA, Littman DR, Ransohoff RM (2006) Control of microglial neurotoxicity by the fractalkine receptor. Nat Neurosci 9:917-924. CrossRef Medline
7. El Khoury JB, Moore KJ, Means TK, Leung J, Terada K, Toft M, Freeman MW, LusterAD (2003) CD36 mediates the innate host response to betaamyloid. J Exp Med 197:1657-1666. CrossRef Medline
8. Field R, Campion S, Warren C, Murray C, Cunningham C (2010) Systemic challenge with the TLR3 agonist poly I:C induces amplified IFNalpha/beta and IL-1beta responses in the diseased brain and exacerbates chronic neurodegeneration. Brain Behav Immun 24:996-1007. CrossRef Medline
9. Glass CK, Saijo K, Winner B, Marchetto MC, Gage FH (2010) Mechanisms underlying inflammation in neurodegeneration. Cell 140:918-934. CrossRef Medline
10. Halle A, Hornung V, Petzold GC, Stewart CR, Monks BG, Reinheckel T, Fitzgerald KA, Latz E, Moore KJ, Golenbock DT (2008) The NALP3 inflammasome is involved in the innate immune response to amyloidbeta. Nat Immunol 9:857-865. CrossRef Medline
11. Hanna RN, Shaked I, Hubbeling HG, Punt JA, Wu R, Herrley E, Zaugg C, Pei H, Geissmann F, Ley K, Hedrick CC (2012) NR4A1 (Nur77) deletion polarizes macrophages toward an inflammatory phenotype and increases atherosclerosis. Circ Res 110:416-427. CrossRef Medline
12. He PP, Zhong Z, Lindholm K, Berning L, Lee W, Lemere C, Staufenbiel M, Li R, Shen Y (2007) Deletion of tumor necrosis factor death receptor inhibits amyloid beta generation and prevents learning and memory deficits in Alzheimer's mice. J Cell Biol 178:829-841. CrossRef Medline
13. Hebert LE, Scherr PA, Bienias JL, Bennett DA, Evans DA (2003) Alzheimer disease in the US population: prevalence estimates using the 2000 census. Arch Neurol 60:1119-1122. CrossRef Medline
14. Heneka MT, O'Banion MK (2007) Inflammatory processes in Alzheimer's disease. J Neuroimmunol 184:69-91. CrossRef Medline
15. Hickman SE, Allison EK, El Khoury J (2008) Microglial dysfunction and defective beta-amyloid clearance pathways in aging Alzheimer's disease mice. J Neurosci 28:8354-8360. CrossRef Medline
16. Honda K, Yanai H, Negishi H, Asagiri M, Sato M, Mizutani T, Shimada N, Ohba Y, Takaoka A, Yoshida N, Taniguchi T (2005) IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 434: 772-777. CrossRef Medline
17. Honda K, Takaoka A, Taniguchi T (2006) Type I interferon gene induction by the interferon regulatory factor family of transcription factors. Immunity 25:349-360. CrossRef Medline
18. 2 stimulates the production of amyloid-beta peptides through internalization of the EP4 receptor. J Biol Chem 284:18493-18502. CrossRef Medline
19. da Huang W, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4:44-57. CrossRef Medline
20. int'Veld BA, Ruitenberg A, Hofman A, Launer LJ, van Duijn CM, Stijnen T, Breteler MM, Stricker BH (2001) Nonsteroidal antiinflammatory drugs and the risk of Alzheimer's disease. N Engl J Med 345:1515-1521. CrossRef Medline
21. Jankowsky JL, Slunt HH, Ratovitski T, Jenkins NA, Copeland NG, Borchelt DR (2001) Co-expression of multiple transgenes in mouse CNS: a comparison of strategies. Biomol Eng 17:157-165. CrossRef Medline
22. Jiang Q, Lee CY, Mandrekar S, Wilkinson B, Cramer P, Zelcer N, Mann K, Lamb B, Willson TM, Collins JL, Richardson JC, Smith JD, Comery TA, Riddell D, Holtzman DM, Tontonoz P, Landreth GE (2008) ApoE promotes the proteolytic degradation of Abeta. Neuron 58:681-693. CrossRef Medline
23. 2 EP2 receptor in macrophages and brain microglia. J Neurosci 33:16016-16032. CrossRef Medline
24. Kabashima K, Saji T, Murata T, Nagamachi M, Matsuoka T, Segi E, Tsuboi K, Sugimoto Y, Kobayashi T, Miyachi Y, Ichikawa A, Narumiya S (2002) The prostaglandin receptor EP4 suppresses colitis, mucosal damage and CD4 cell activation in the gut. J Clin Invest 109:883-893. CrossRef Medline
25. Krabbe G, Halle A, Matyash V, Rinnenthal JL, Eom GD, Bernhardt U, Miller KR, Prokop S, Kettenmann H, Heppner FL (2013) Functional impairment of microglia coincides with Beta-amyloid deposition in mice with Alzheimer-like pathology. PLoS One 8:e60921. CrossRef Medline
26. Landreth GE, Reed-Geaghan EG (2009) Toll-like receptors in Alzheimer's disease. In: Current topics in microbiology and immunology, pp 137-153. Berlin: Springer.
27. Lee S, Varvel NH, Konerth ME, Xu G, Cardona AE, Ransohoff RM, Lamb BT (2010) CX3CR1 deficiency alters microglial activation and reduces betaamyloid deposition in two Alzheimer's disease mouse models. Am J Pathol 177:2549-2562. CrossRef Medline
28. Lesné S, Koh MT, Kotilinek L, Kayed R, Glabe CG, Yang A, Gallagher M, Ashe KH (2006) A specific amyloid-beta protein assembly in the brain impairs memory. Nature 440:352-357. CrossRef Medline
29. 2 EP2 receptor reduces oxidative damage and amyloid burden in a model of Alzheimer's disease. J Neurosci 25:10180-10187. CrossRef Medline
30. Liang X, Lin L, Woodling NS, Wang Q, Anacker C, Pan T, Merchant M, Andreasson K (2011) Signaling via the prostaglandin E(2) receptor EP4 exerts neuronal and vascular protection in a mouse model of cerebral ischemia. J Clin Invest 121:4362-4371. CrossRef Medline
31. Marié I, Durbin JE, Levy DE (1998) Differential viral induction of distinct interferon-alpha genes by positive feedback through interferon regulatory factor-7. EMBO J 17:6660-6669. CrossRef Medline
32. McGeer PL, McGeer EG (2007) NSAIDs and Alzheimer disease: epidemiological, animal model and clinical studies. Neurobiol Aging 28:639-647. CrossRef Medline
33. Minami M, Shimizu K, Okamoto Y, Folco E, Ilasaca ML, Feinberg MW, Aikawa M, Libby P (2008) Prostaglandin E receptor type 4-associated protein interacts directly with NF-kappaB1 and attenuates macrophage activation. J Biol Chem 283:9692-9703. CrossRef Medline
34. Nguyen M, Camenisch T, Snouwaert JN, Hicks E, Coffman TM, Anderson PA, Malouf NN, Koller BH (1997) The prostaglandin receptor EP4 triggers remodelling of the cardiovascular system at birth. Nature 390:78-81. CrossRef Medline
35. Passos GF, Figueiredo CP, Prediger RDS, Pandolfo P, Duarte FS, Medeiros R, Calixto JB (2009) Role of the macrophage inflammatory protein-1alpha/ CC chemokine receptor 5 signaling pathway in the neuroinflammatory response and cognitive deficits induced by beta-amyloid peptide. J Pathol 175:1586-1597. CrossRef Medline
36. Saijo K, Winner B, Carson CT, Collier JG, Boyer L, Rosenfeld MG, Gage FH, Glass CK (2009) A Nurr1/CoREST pathway in microglia and astrocytes protects dopaminergic neurons from inflammation-induced death. Cell 137:47-59. CrossRef Medline
37. Schneider A, Guan Y, Zhang Y, Magnuson MA, Pettepher C, Loftin CD, Langenbach R, Breyer RM, Breyer MD (2004) Generation of a conditional allele of the mouse prostaglandin EP4 receptor. Genesis 40:7-14. CrossRef Medline
38. 2 E-prostanoid 4 receptor exerts anti-inflammatory effects in brain innate immunity. J Immunol 184:7207-7218. CrossRef Medline
39. Shi J, Wang Q, Johansson JU, Liang X, Woodling NS, Priyam P, Loui TM, Merchant M, Breyer RM, Montine TJ, Andreasson K (2012) Inflammatory prostaglandin E(2) signaling in a mouse model of Alzheimer disease. Ann Neurol 72:788-798. CrossRef Medline
40. Shie FS, Breyer RM, Montine TJ (2005a) Microglia lacking E prostanoid receptor subtype 2 have enhanced Abeta phagocytosis yet lack Abetaactivated neurotoxicity. J Pathol 166:1163-1172. CrossRef Medline
41. Shie FS, Montine KS, Breyer RM, Montine TJ (2005b) Microglial EP2 is critical to neurotoxicity from activated cerebral innate immunity. Glia 52:70-77. CrossRef Medline
42. Spandidos A, Wang X, Wang H, Seed B (2010) PrimerBank: a resource of human and mouse PCR primer pairs for gene expression detection and quantification. Nucleic Acids Res 38:D792-D799. CrossRef Medline
43. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP (2005) Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A 102: 15545-15550. CrossRef Medline
44. Suzawa T, Miyaura C, Inada M, Maruyama T, Sugimoto Y, Ushikubi F, Ichikawa A, Narumiya S, Suda T (2000) The role of prostaglandin E receptor subtypes (EP1, EP2, EP3, and EP4) in bone resorption: an analysis using specific agonists for the respective EPs. Endocrinology 141: 1554-1559. CrossRef Medline
45. Vlad SC, Miller DR, Kowall NW, Felson DT (2008) Protective effects of NSAIDs on the development of Alzheimer disease. Neurology 70:1672-1677. CrossRef Medline
46. Vom Berg J, Prokop S, Miller KR, Obst J, Kälin RE, Lopategui-Cabezas I, Wegner A, Mair F, Schipke CG, Peters O, Winter Y, Becher B, Heppner FL (2012) Inhibition of IL-12/IL-23 signaling reduces Alzheimer's disease-like pathology and cognitive decline. Nat Med 18:1812-1819. CrossRef Medline
47. Wang R, Yang B, Zhang D (2011) Activation of interferon signaling pathways in spinal cord astrocytes from an ALS mouse model. Glia 59:946-958. CrossRef Medline
48. Wyss-Coray T (2006) Inflammation in Alzheimer disease: driving force, bystander or beneficial response? Nat Med 12:1005-1015. Medline
49. Yang T, Knowles JK, Lu Q, Zhang H, Arancio O, Moore LA, Chang T, Wang Q, Andreasson K, Rajadas J, Fuller GG, Xie Y, Massa SM, Longo FM (2008) Small molecule, non-peptide p75 ligands inhibit Abeta-induced neurodegeneration and synaptic impairment. PLoS One 3:e3604. CrossRef Medline
50. Zagol-Ikapitte I, Masterson TS, Amarnath V, Montine TJ, Andreasson KI, Boutaud O, Oates JA (2005) Prostaglandin H(2)-derived adducts of proteins correlate with Alzheimer's disease severity. J Neurochem 94: 1140-1145. CrossRef Medline
51. 2 EP1 receptor exacerbated neurotoxicity in a mouse model of cerebral ischemia and Alzheimer's disease. Neurobiol Aging 33:2215-2219. CrossRef Medline