Brain-derived neurotrophic factor-dependent synaptic plasticity is suppressed by interleukin-1β via p38 mitogen-activated protein kinase

Journal of Neuroscience

Volumn 32, Issue 49, 2012, Pages 17714-17724

  Tong, Liqi ^a   Aleph Prieto, G ^a   Kramár, Enikö A ^b   Smith, Erica D ^a   Cribbs, David H ^a   Lynch, Gary ^b   Cotman, Carl W ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; COFILIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; INSULIN RECEPTOR SUBSTRATE 1; INTERLEUKIN 1BETA; MICROTUBULE ASSOCIATED PROTEIN 2; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN HOMER 1A; PROTEIN KINASE B;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENDRITIC SPINE; ELECTROPHYSIOLOGY; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; IMMUNOPRECIPITATION; LONG TERM POTENTIATION; MALE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING;

ACTINS; ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELLS, CULTURED; CEREBRAL CORTEX; COFILIN 1; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; CYTOSKELETAL PROTEINS; EXCITATORY POSTSYNAPTIC POTENTIALS; GENE EXPRESSION REGULATION; HIPPOCAMPUS; INTERLEUKIN-1BETA; LONG-TERM POTENTIATION; MALE; MITOGEN-ACTIVATED PROTEIN KINASES; NERVE TISSUE PROTEINS; NEURONAL PLASTICITY; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION;

EID: 84870524516     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1253-12.2012     Document Type: Article

References (69)

1. Adlard PA, Perreau VM, Engesser-Cesar C, Cotman CW (2004) The timecourse of induction of brain-derived neurotrophic factormRNAand protein in the rat hippocampus following voluntary exercise. Neurosci Lett 363:43-48.CrossRef Medline
2. Aid T, Kazantseva A, Piirsoo M, Palm K, Timmusk T (2007) Mouse and rat BDNF gene structure and expression revisited. J Neurosci Res 85:525-535.CrossRef Medline
3. Barrientos RM, Frank MG, Hein AM, Higgins EA, Watkins LR, Rudy JW, Maier SF (2009) Time course of hippocampal IL-1 beta and memory consolidation impairments in aging rats following peripheral infection. Brain Behav Immun 23:46-54.CrossRef Medline
4. Bellinger FP, Madamba S, Siggins GR (1993) Interleukin 1 beta inhibits synaptic strength and long-term potentiation in the rat CA1 hippocampus. Brain Res 628:227-234.CrossRef Medline
5. Böni-Schnetzler M, Donath MY (2011) Increased IL-1beta activation, the culprit not only for defective insulin secretion but also for insulin resistance? Cell Res 21:995-997.CrossRef Medline
6. Bramham CR (2008) Local protein synthesis, actin dynamics, and LTP consolidation. Curr Opin Neurobiol 18:524-531.CrossRef Medline
7. Bramham CR, Alme MN, Bittins M, Kuipers SD, Nair RR, Pai B, Panja D, Schubert M, Soule J, Tiron A, Wibrand K (2010) The Arc of synaptic memory. Exp Brain Res 200:125-140.CrossRef Medline
8. Cacabelos R, Barquero M, García P, Alvarez XA, Varela de Seijas E (1991) Cerebrospinal fluid interleukin-1 beta (IL-1 beta) in Alzheimer's disease and neurological disorders. Methods Find Exp Clin Pharmacol 13:455-458. Medline
9. Chang FY, Lee CC, Huang CC, Hsu KS (2009) Unconjugated bilirubin exposure impairs hippocampal long-term synaptic plasticity. PLoS One 4:e5876.CrossRef Medline
10. Chapman TR, Barrientos RM, Ahrendsen JT, Maier SF, Patterson SL (2010) Synaptic correlates of increased cognitive vulnerability with aging: peripheral immune challenge and aging interact to disrupt theta-burst latephase long-term potentiation in hippocampal area CA1. J Neurosci 30: 7598-7603.CrossRef Medline
11. Chapman TR, Barrientos RM, Ahrendsen JT, Hoover JM, Maier SF, Patterson SL (2011) Aging and infection reduce expression of specific brainderived neurotrophic factor mRNAs in hippocampus. Neurobiol Aging 33:832.e1-e14.CrossRef Medline
12. Chen LY, Rex CS, Sanaiha Y, Lynch G, Gall CM (2010) Learning induces neurotrophin signaling at hippocampal synapses. Proc Natl Acad Sci U S A 107:7030-7035.CrossRef Medline
13. Chen TJ, Wang DC, Chen SS (2009) Amyloid-beta interrupts the PI3K-AktmTOR signaling pathway that could be involved in brain-derived neurotrophic factor-induced Arc expression in rat cortical neurons. J Neurosci Res 87:2297-2307.CrossRef Medline
14. Curran BP, Murray HJ, O'Connor JJ (2003) A role for c-Jun N-terminal kinase in the inhibition of long-term potentiation by interleukin-1beta and long-term depression in the rat dentate gyrus in vitro. Neuroscience 118:347-357.CrossRef Medline
15. Davis S, Laroche S (2006) Mitogen-activated protein kinase/extracellular regulated kinase signalling and memory stabilization: a review. Genes Brain Behav 5 [Suppl 2]:61-72. CrossRef
16. Du K, Montminy M (1998) CREB is a regulatory target for the protein kinase Akt/PKB. J Biol Chem 273:32377-32379.CrossRef Medline
17. Erickson KI, Prakash RS, Voss MW, Chaddock L, Heo S, McLaren M, Pence BD, Martin SA, Vieira VJ, Woods JA, McAuley E, Kramer AF (2010) Brain-derived neurotrophic factor is associated with age-related decline in hippocampal volume. J Neurosci 30:5368-5375.CrossRef Medline
18. Figurov A, Pozzo-Miller LD, Olafsson P, Wang T, Lu B (1996) Regulation of synaptic responses to high-frequency stimulation and LTP by neurotrophins in the hippocampus. Nature 381:706-709.CrossRef Medline
19. Frank MG, Barrientos RM, Hein AM, Biedenkapp JC, Watkins LR, Maier SF (2010) IL-1RA blocks E. coli-induced suppression of Arc and long-term memory in aged F344xBN F1 rats. Brain Behav Immun 24:254-262.CrossRef Medline
20. Gallagher SM, Daly CA, Bear MF, Huber KM (2004) Extracellular signalregulated protein kinase activation is required for metabotropic glutamate receptor-dependent long-term depression in hippocampal area CA1. J Neurosci 24:4859-4864.CrossRef Medline
21. García-San Frutos M, Fernández-Agullo ́ T, Carrascosa JM, Horrillo D, Barrus MT, Oliveros E, Sierra J, Ros M (2012) Involvement of protein tyrosine phosphatases and inflammation in hypothalamic insulin resistance associated with ageing: effect of caloric restriction. Mech Ageing Dev 133: 489-497.CrossRef Medline
22. Hein AM, Stasko MR, Matousek SB, Scott-McKean JJ, Maier SF, Olschowka JA, Costa AC, O'Banion MK (2010) Sustained hippocampal IL-1beta overexpression impairs contextual and spatial memory in transgenic mice. Brain Behav Immun 24:243-253.CrossRef Medline
23. Hemi R, Yochananov Y, Barhod E, Kasher-Meron M, Karasik A, Tirosh A, Kanety H (2011) P38 mitogen-activated protein kinase-dependent transactivation of ErbB receptor family: a novel common mechanism for stress-induced IRS-1 serine phosphorylation and insulin resistance. Diabetes 60:1134-1145.CrossRef Medline
24. Hsieh H, Boehm J, Sato C, Iwatsubo T, Tomita T, Sisodia S, Malinow R (2006) AMPAR removal underlies Abeta-induced synaptic depression and dendritic spine loss. Neuron 52:831-843.CrossRef Medline
25. Huang EJ, Reichardt LF (2003) Trk receptors: roles in neuronal signal transduction. Annu Rev Biochem 72:609-642.CrossRef Medline
26. Kawashima T, Okuno H, Nonaka M, Adachi-Morishima A, Kyo N, Okamura M, Takemoto-Kimura S, Worley PF, Bito H (2009) Synaptic activityresponsive element in the Arc/Arg3.1 promoter essential for synapse-tonucleus signaling in activated neurons. Proc Natl Acad Sci U S A 106: 316-321.CrossRef Medline
27. Kim SH, Smith CJ, Van Eldik LJ (2004) Importance of MAPK pathways for microglial pro-inflammatory cytokine IL-1 beta production. Neurobiol Aging 25:431-439.CrossRef Medline
28. Korte M, Carroll P, Wolf E, Brem G, Thoenen H, Bonhoeffer T (1995) Hippocampal long-term potentiation is impaired in mice lacking brain- derived neurotrophic factor. Proc Natl Acad Sci U S A 92:8856-8860.CrossRef Medline
29. Kramár EA, Lin B, Lin CY, Arai AC, Gall CM, Lynch G (2004) A novel mechanism for the facilitation of theta-induced long-term potentiation by brain-derived neurotrophic factor. J Neurosci 24:5151-5161. CrossRef Medline
30. Kramár EA, Lin B, Rex CS, Gall CM, Lynch G (2006) Integrin-driven actin polymerization consolidates long-term potentiation. Proc Natl Acad Sci U S A 103:5579-5584.CrossRef Medline
31. Larson J, Wong D, Lynch G (1986) Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation. Brain Res 368:347-350.CrossRef Medline
32. Li G, Peskind ER, Millard SP, Chi P, Sokal I, Yu CE, Bekris LM, Raskind MA, Galasko DR, Montine TJ (2009) Cerebrospinal fluid concentration of brain-derived neurotrophic factor and cognitive function in nondemented subjects. PLoS One 4:e5424.CrossRef Medline
33. Lin B, Kramár EA, Bi X, Brucher FA, Gall CM, Lynch G (2005) Theta stimulation polymerizes actin in dendritic spines of hippocampus. J Neurosci 25:2062-2069.CrossRef Medline
34. Liu IY, Lyons WE, Mamounas LA, Thompson RF (2004) Brain-derived neurotrophic factor plays a critical role in contextual fear conditioning. J Neurosci 24:7958-7963.CrossRef Medline
35. Marette A (2002) Mediators of cytokine-induced insulin resistance in obesity and other inflammatory settings. Curr Opin Clin Nutr Metab Care 5:377-383.CrossRef Medline
36. Messaoudi E, Kanhema T, Soulé J, Tiron A, Dagyte G, da Silva B, Bramham CR (2007) Sustained Arc/Arg3.1 synthesis controls long-term potentiation consolidation through regulation of local actin polymerization in the dentate gyrus in vivo. J Neurosci 27:10445-10455.CrossRef Medline
37. Minami I, Kengaku M, Smitt PS, Shigemoto R, Hirano T (2003) Long-term potentiation of mGluR1 activity by depolarization-induced Homer1a in mouse cerebellar Purkinje neurons. Eur J Neurosci 17:1023-1032.CrossRef Medline
38. Minichiello L, Casagranda F, Tatche RS, Stucky CL, Postigo A, Lewin GR, Davies AM, Klein R (1998) Point mutation in trkB causes loss of NT4- dependent neurons without major effects on diverse BDNF responses. Neuron 21:335-345.CrossRef Medline
39. Olefsky JM, Glass CK (2010) Macrophages, inflammation, and insulin resistance. Annu Rev Physiol 72:219-246.CrossRef Medline
40. Opazo P, Watabe AM, Grant SG, O'Dell TJ (2003) Phosphatidylinositol 3-kinase regulates the induction of long-term potentiation through extracellular signal-related kinase-independent mechanisms. J Neurosci 23: 3679-3688. Medline
41. Origlia N, Righi M, Capsoni S, Cattaneo A, Fang F, Stern DM, Chen JX, Schmidt AM, Arancio O, Yan SD, Domenici L (2008) Receptor for advanced glycation end product-dependent activation of p38 mitogenactivated protein kinase contributes to amyloid-β-mediated cortical synaptic dysfunction. J Neurosci 28:3521-3530.CrossRef Medline
42. Pena F (2010) Organotypic cultures as tool to test long-term effects of chemicals on the nervous system. Curr Med Chem 17:987-1001. CrossRef Medline
43. Peng S, Wuu J, Mufson EJ, Fahnestock M (2005) Precursor form of brainderived neurotrophic factor and mature brain-derived neurotrophic factor are decreased in the pre-clinical stages of Alzheimer's disease. J Neurochem 93:1412-1421.CrossRef Medline
44. Pinteaux E, Trotter P, Simi A (2009) Cell-specific and concentrationdependent actions of interleukin-1 in acute brain inflammation. Cytokine 45:1-7.CrossRef Medline
45. Rachal Pugh C, Fleshner M, Watkins LR, Maier SF, Rudy JW (2001) Theimmune system and memory consolidation: a role for the cytokine IL-1beta. Neurosci Biobehav Rev 25:29-41.CrossRef Medline
46. Rex CS, Lin CY, Kramár EA, Chen LY, Gall CM, Lynch G (2007) Brainderived neurotrophic factor promotes long-term potentiation-related cytoskeletal changes in adult hippocampus. J Neurosci 27:3017-3029.CrossRef Medline
47. Ross FM, Allan SM, Rothwell NJ, Verkhratsky A (2003) A dual role for interleukin-1 in LTP in mouse hippocampal slices. J Neuroimmunol 144: 61-67.CrossRef Medline
48. Rothwell NJ, Luheshi GN (2000) Interleukin 1 in the brain: biology, pathology and therapeutic target. Trends Neurosci 23:618-625.CrossRef Medline
49. Rush AM, Wu J, Rowan MJ, Anwyl R (2002) Group I metabotropic glutamate receptor (mGluR)-dependent long-term depression mediated via p38 mitogen-activated protein kinase is inhibited by previous highfrequency stimulation and activation of mGluRs and protein kinase C in the rat dentate gyrus in vitro. J Neurosci 22:6121-6128. Medline
50. Sala C, Futai K, Yamamoto K, Worley PF, Hayashi Y, Sheng M (2003) Inhibition of dendritic spine morphogenesis and synaptic transmission by activity-inducible protein Homer1a. J Neurosci 23:6327-6337. Medline
51. Sanna PP, Cammalleri M, Berton F, Simpson C, Lutjens R, Bloom FE, Francesconi W (2002) Phosphatidylinositol 3-kinase is required for the expression but not for the induction or the maintenance of long-term potentiation in the hippocampal CA1 region. J Neurosci 22:3359-3365. Medline
52. Sato M, Suzuki K, Nakanishi S (2001) NMDA receptor stimulation and brain-derived neurotrophic factor upregulate homer 1a mRNA via the mitogen-activated protein kinase cascade in cultured cerebellar granule cells. J Neurosci 21:3797-3805. Medline
53. Shepherd JD, Bear MF (2011) New views of Arc, a master regulator of synaptic plasticity. Nat Neurosci 14:279-284.CrossRef Medline
54. Simão F, Matté A, Pagnussat AS, Netto CA, Salbego CG (2012) Resveratrol prevents CA1 neurons against ischemic injury by parallel modulation of both GSK-3β and CREB through PI3-K/Akt pathways. Eur J Neurosci 36:2899-2905.CrossRef Medline
55. Srinivasan D, Yn JH, Joseph DJ, Friedman W (2004) Cell type-specific interleukin-1β signaling in the CNS. J Neurosci 24:6482-6488.CrossRef Medline
56. Stoppini L, Buchs PA, Muller D (1991) A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 37:173-182. CrossRef Medline
57. Størling J, Zaitsev SV, Kapelioukh IL, Karlsen AE, Billestrup N, Berggren PO, Mandrup-Poulsen T (2005) Calcium has a permissive role in interleukin-1beta-induced c-jun N-terminal kinase activation in insulinsecreting cells. Endocrinology 146:3026-3036.CrossRef Medline
58. Tanaka J, Horiike Y, Matsuzaki M, Miyazaki T, Ellis-Davies GC, Kasai H (2008) Protein synthesis and neurotrophin-dependent structural plasticity of single dendritic spines. Science 319:1683-1687.CrossRef Medline
59. Tao X, Finkbeiner S, Arnold DB, Shaywitz AJ, Greenberg ME (1998) Ca2 influx regulates BDNF transcription by a CREB family transcription factor-dependent mechanism. Neuron [Erratum (1998) 20:1297] 20: 709-726.CrossRef Medline
60. Tapia-Arancibia L, Aliaga E, Silhol M, Arancibia S (2008) New insights into brain BDNF function in normal aging and Alzheimer disease. Brain Res Rev 59:201-220.CrossRef Medline
61. Thibault O, Hadley R, Landfield PW (2001) Elevated postsynaptic [Ca 2 ]I and L-type calcium channel activity in aged hippocampal neurons: relationship to impaired synaptic plasticity. J Neurosci 21:9744-9756. Medline
62. Tong L, Thornton PL, Balazs R, Cotman CW (2001) Beta-amyloid-(1-42) impairs activity-dependent cAMP-response element-binding protein signaling in neurons at concentrations in which cell survival is not compromised. J Biol Chem 276:17301-17306.CrossRef Medline
63. Tong L, Balazs R, Soiampornkul R, Thangnipon W, Cotman CW (2008) Interleukin-1 beta impairs brain derived neurotrophic factor-induced signal transduction. Neurobiol Aging 29:1380-1393.CrossRef Medline
64. Vereker E, Campbell V, Roche E, McEntee E, Lynch MA (2000) Lipopolysaccharide inhibits long term potentiation in the rat dentate gyrus by activating caspase-1. J Biol Chem 275:26252-26258.CrossRef Medline
65. Viviani B, Bartesaghi S, Gardoni F, Vezzani A, Behrens MM, Bartfai T, Binaglia M, Corsini E, Di Luca M, Galli CL, Marinovich M (2003) Interleukin-1beta enhances NMDA receptor-mediated intracellular calcium increase through activation of the Src family of kinases. J Neurosci 23:8692-8700. Medline
66. Wang Q, Walsh DM, Rowan MJ, Selkoe DJ, Anwyl R (2004) Block of longterm potentiation by naturally secreted and synthetic amyloid betapeptide in hippocampal slices is mediated via activation of the kinases c-Jun N-terminal kinase, cyclin-dependent kinase 5, and p38 mitogenactivated protein kinase as well as metabotropic glutamate receptor type 5. J Neurosci 24:3370-3378.CrossRef Medline
67. Yao WD, Spealman RD, Zhang J (2008) Dopaminergic signaling in dendritic spines. Biochem Pharmacol 75:2055-2069.CrossRef Medline
68. Yin Y, Edelman GM, Vanderklish PW (2002) The brain-derived neurotrophic factor enhances synthesis of Arc in synaptoneurosomes. Proc Natl Acad Sci U S A 99:2368-2373.CrossRef Medline
69. Zick Y (2001) Insulin resistance: a phosphorylation-based uncoupling of insulin signaling. Trends Cell Biol [Erratum (2002) 12:56] 11:437-441.CrossRef Medline