Neuroinflammatory TNFα Impairs Memory via Astrocyte Signaling

Cell

Volumn 163, Issue 7, 2015, Pages 1730-1741

  Habbas, Samia ^a   Santello, Mirko ^a,f   Becker, Denise ^a   Stubbe, Hiltrud ^a   Zappia, Giovanna ^a   Liaudet, Nicolas ^a   Klaus, Federica R ^b   Kollias, George ^c   Fontana, Adriano ^d   Pryce, Christopher R ^b   Suter, Tobias ^e   Volterra, Andrea ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b UNIVERSITY HOSPITAL OF PSYCHIATRY   (Switzerland)

^c BIOMEDICAL SCIENCES RESEARCH CENTER ALEXANDER FLEMING   (Greece)

^d UNIVERSITY OF ZURICH   (Switzerland)

^e UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^f UNIVERSITY OF BERN   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

IFENPRODIL; MOLECULAR LAYER; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PIPERIDINE DERIVATIVE; TNFRSF1A PROTEIN, MOUSE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; COGNITIVE DEFECT; CONCENTRATION RESPONSE; CONTROLLED STUDY; DENTATE GYRUS; EXPERIMENTAL ALLERGIC ENCEPHALITIS; HIPPOCAMPUS; LEARNING; MEMORY DISORDER; MOTOR PERFORMANCE; MOUSE; MULTIPLE SCLEROSIS; NERVOUS SYSTEM INFLAMMATION; NEUROPATHOLOGY; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ANIMAL; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; HUMAN; IMMUNOLOGY; MEMORY; METABOLISM; PATHOPHYSIOLOGY;

ANIMALS; ASTROCYTES; DENTATE GYRUS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; HUMANS; LEARNING; MEMORY; MICE; MULTIPLE SCLEROSIS; PIPERIDINES; RECEPTORS, N-METHYL-D-ASPARTATE; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE I; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84950288379     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2015.11.023     Document Type: Article

References (52)

1. S. Acharjee, N. Nayani, M. Tsutsui, M.N. Hill, S.S. Ousman, and Q.J. Pittman Altered cognitive-emotional behavior in early experimental autoimmune encephalitis - cytokine and hormonal correlates Brain Behav. Immun. 33 2013 164 172
2. S.G. Anagnostaras, G.D. Gale, and M.S. Fanselow Hippocampus and contextual fear conditioning: recent controversies and advances Hippocampus 11 2001 8 17
3. A. Araque, G. Carmignoto, P.G. Haydon, S.H. Oliet, R. Robitaille, and A. Volterra Gliotransmitters travel in time and space Neuron 81 2014 728 739
4. E.C. Beattie, D. Stellwagen, W. Morishita, J.C. Bresnahan, B.K. Ha, M. Von Zastrow, M.S. Beattie, and R.C. Malenka Control of synaptic strength by glial TNFalpha Science 295 2002 2282 2285
5. K. Belarbi, T. Jopson, D. Tweedie, C. Arellano, W. Luo, N.H. Greig, and S. Rosi TNF-α protein synthesis inhibitor restores neuronal function and reverses cognitive deficits induced by chronic neuroinflammation J. Neuroinflammation 9 2012 23
6. P. Bezzi, M. Domercq, L. Brambilla, R. Galli, D. Schols, E. De Clercq, A. Vescovi, G. Bagetta, G. Kollias, J. Meldolesi, and A. Volterra CXCR4-activated astrocyte glutamate release via TNFalpha: amplification by microglia triggers neurotoxicity Nat. Neurosci. 4 2001 702 710
7. D. Centonze, L. Muzio, S. Rossi, F. Cavasinni, V. De Chiara, A. Bergami, A. Musella, M. D'Amelio, V. Cavallucci, A. Martorana, and et al. Inflammation triggers synaptic alteration and degeneration in experimental autoimmune encephalomyelitis J. Neurosci. 29 2009 3442 3452
8. P.F. Chapman, G.L. White, M.W. Jones, D. Cooper-Blacketer, V.J. Marshall, M. Irizarry, L. Younkin, M.A. Good, T.V. Bliss, B.T. Hyman, and et al. Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice Nat. Neurosci. 2 1999 271 276
9. N.D. Chiaravalloti, and J. DeLuca Cognitive impairment in multiple sclerosis Lancet Neurol. 7 2008 1139 1151
10. I.A. Clark, L.M. Alleva, and B. Vissel The roles of TNF in brain dysfunction and disease Pharmacol. Ther. 128 2010 519 548
11. L. Codarri, G. Gyülvészi, V. Tosevski, L. Hesske, A. Fontana, L. Magnenat, T. Suter, and B. Becher RORγt drives production of the cytokine GM-CSF in helper T cells, which is essential for the effector phase of autoimmune neuroinflammation Nat. Immunol. 12 2011 560 567
12. A.J. Cunningham, C.A. Murray, L.A. O'Neill, M.A. Lynch, and J.J. O'Connor Interleukin-1 beta (IL-1 beta) and tumour necrosis factor (TNF) inhibit long-term potentiation in the rat dentate gyrus in vitro Neurosci. Lett. 203 1996 17 20
13. C.A. Denny, M.A. Kheirbek, E.L. Alba, K.F. Tanaka, R.A. Brachman, K.B. Laughman, N.K. Tomm, G.F. Turi, A. Losonczy, and R. Hen Hippocampal memory traces are differentially modulated by experience, time, and adult neurogenesis Neuron 83 2014 189 201
14. M. Domercq, L. Brambilla, E. Pilati, J. Marchaland, A. Volterra, and P. Bezzi P2Y1 receptor-evoked glutamate exocytosis from astrocytes: control by tumor necrosis factor-alpha and prostaglandins J. Biol. Chem. 281 2006 30684 30696
15. H.P. Eugster, K. Frei, R. Bachmann, H. Bluethmann, H. Lassmann, and A. Fontana Severity of symptoms and demyelination in MOG-induced EAE depends on TNFR1 Eur. J. Immunol. 29 1999 626 632
16. S.P. Gabbita, M.K. Srivastava, P. Eslami, M.F. Johnson, N.K. Kobritz, D. Tweedie, N.H. Greig, F.P. Zemlan, S.P. Sharma, and M.E. Harris-White Early intervention with a small molecule inhibitor for tumor necrosis factor-α prevents cognitive deficits in a triple transgenic mouse model of Alzheimer's disease J. Neuroinflammation 9 2012 99
17. S.M. Gold, K.C. Kern, M.F. O'Connor, M.J. Montag, A. Kim, Y.S. Yoo, B.S. Giesser, and N.L. Sicotte Smaller cornu ammonis 2-3/dentate gyrus volumes and elevated cortisol in multiple sclerosis patients with depressive symptoms Biol. Psychiatry 68 2010 553 559
18. I.V. Goussakov, K. Fink, C.E. Elger, and H. Beck Metaplasticity of mossy fiber synaptic transmission involves altered release probability J. Neurosci. 20 2000 3434 3441
19. A.P. Gregory, C.A. Dendrou, K.E. Attfield, A. Haghikia, D.K. Xifara, F. Butter, G. Poschmann, G. Kaur, L. Lambert, O.A. Leach, and et al. TNF receptor 1 genetic risk mirrors outcome of anti-TNF therapy in multiple sclerosis Nature 488 2012 508 511
20. Y. Gu, M. Arruda-Carvalho, J. Wang, S.R. Janoschka, S.A. Josselyn, P.W. Frankland, and S. Ge Optical controlling reveals time-dependent roles for adult-born dentate granule cells Nat. Neurosci. 15 2012 1700 1706
21. N. Haji, G. Mandolesi, A. Gentile, L. Sacchetti, D. Fresegna, S. Rossi, A. Musella, H. Sepman, C. Motta, V. Studer, and et al. TNF-alpha-mediated anxiety in a mouse model of multiple sclerosis Exp. Neurol. 237 2012 296 303
22. M.M. Halassa, C. Florian, T. Fellin, J.R. Munoz, S.Y. Lee, T. Abel, P.G. Haydon, and M.G. Frank Astrocytic modulation of sleep homeostasis and cognitive consequences of sleep loss Neuron 61 2009 213 219
23. J. Han, P. Kesner, M. Metna-Laurent, T. Duan, L. Xu, F. Georges, M. Koehl, D.N. Abrous, J. Mendizabal-Zubiaga, P. Grandes, and et al. Acute cannabinoids impair working memory through astroglial CB1 receptor modulation of hippocampal LTD Cell 148 2012 1039 1050
24. X. Han, M. Chen, F. Wang, M. Windrem, S. Wang, S. Shanz, Q. Xu, N.A. Oberheim, L. Bekar, S. Betstadt, and et al. Forebrain engraftment by human glial progenitor cells enhances synaptic plasticity and learning in adult mice Cell Stem Cell 12 2013 342 353
25. P. He, Z. Zhong, K. Lindholm, L. Berning, W. Lee, C. Lemere, M. Staufenbiel, R. Li, and Y. Shen 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 2007 829 841
26. P.G. Hirrlinger, A. Scheller, C. Braun, J. Hirrlinger, and F. Kirchhoff Temporal control of gene recombination in astrocytes by transgenic expression of the tamoxifen-inducible DNA recombinase variant CreERT2 Glia 54 2006 11 20
27. P. Jourdain, L.H. Bergersen, K. Bhaukaurally, P. Bezzi, M. Santello, M. Domercq, C. Matute, F. Tonello, V. Gundersen, and A. Volterra Glutamate exocytosis from astrocytes controls synaptic strength Nat. Neurosci. 10 2007 331 339
28. G. Kassiotis, and G. Kollias Uncoupling the proinflammatory from the immunosuppressive properties of tumor necrosis factor (TNF) at the p55 TNF receptor level: implications for pathogenesis and therapy of autoimmune demyelination J. Exp. Med. 193 2001 427 434
29. R.S. Larsen, R.J. Corlew, M.A. Henson, A.C. Roberts, M. Mishina, M. Watanabe, S.A. Lipton, N. Nakanishi, I. Pérez-Otaño, R.J. Weinberg, and B.D. Philpot NR3A-containing NMDARs promote neurotransmitter release and spike timing-dependent plasticity Nat. Neurosci. 14 2011 338 344
30. H.S. Lee, A. Ghetti, A. Pinto-Duarte, X. Wang, G. Dziewczapolski, F. Galimi, S. Huitron-Resendiz, J.C. Piña-Crespo, A.J. Roberts, I.M. Verma, and et al. Astrocytes contribute to gamma oscillations and recognition memory Proc. Natl. Acad. Sci. USA 111 2014 E3343 E3352
31. X. Liu, S. Ramirez, P.T. Pang, C.B. Puryear, A. Govindarajan, K. Deisseroth, and S. Tonegawa Optogenetic stimulation of a hippocampal engram activates fear memory recall Nature 484 2012 381 385
32. F.E. McAlpine, and M.G. Tansey Neuroinflammation and tumor necrosis factor signaling in the pathophysiology of Alzheimer's disease J. Inflamm. Res. 1 2008 29 39
33. P. Paoletti, C. Bellone, and Q. Zhou NMDA receptor subunit diversity: impact on receptor properties, synaptic plasticity and disease Nat. Rev. Neurosci. 14 2013 383 400
34. O. Pascual, K.B. Casper, C. Kubera, J. Zhang, R. Revilla-Sanchez, J.Y. Sul, H. Takano, S.J. Moss, K. McCarthy, and P.G. Haydon Astrocytic purinergic signaling coordinates synaptic networks Science 310 2005 113 116
35. H. Pribiag, and D. Stellwagen TNF-α downregulates inhibitory neurotransmission through protein phosphatase 1-dependent trafficking of GABA(A) receptors J. Neurosci. 33 2013 15879 15893
36. T. Renno, M. Krakowski, C. Piccirillo, J.Y. Lin, and T. Owens TNF-alpha expression by resident microglia and infiltrating leukocytes in the central nervous system of mice with experimental allergic encephalomyelitis. Regulation by Th1 cytokines J. Immunol. 154 1995 944 953
37. J. Rothe, W. Lesslauer, H. Lötscher, Y. Lang, P. Koebel, F. Köntgen, A. Althage, R. Zinkernagel, M. Steinmetz, and H. Bluethmann Mice lacking the tumour necrosis factor receptor 1 are resistant to TNF-mediated toxicity but highly susceptible to infection by Listeria monocytogenes Nature 364 1993 798 802
38. M. Santello, and A. Volterra TNFα in synaptic function: switching gears Trends Neurosci. 35 2012 638 647
39. M. Santello, P. Bezzi, and A. Volterra TNFα controls glutamatergic gliotransmission in the hippocampal dentate gyrus Neuron 69 2011 988 1001
40. S. Srinivas, T. Watanabe, C.S. Lin, C.M. William, Y. Tanabe, T.M. Jessell, and F. Costantini Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus BMC Dev. Biol. 1 2001 4
41. D. Stellwagen, E.C. Beattie, J.Y. Seo, and R.C. Malenka Differential regulation of AMPA receptor and GABA receptor trafficking by tumor necrosis factor-alpha J. Neurosci. 25 2005 3219 3228
42. A. Suzuki, S.A. Stern, O. Bozdagi, G.W. Huntley, R.H. Walker, P.J. Magistretti, and C.M. Alberini Astrocyte-neuron lactate transport is required for long-term memory formation Cell 144 2011 810 823
43. W. Swardfager, and S.E. Black Dementia: A link between microbial infection and cognition? Nat. Rev. Neurol. 9 2013 301 302
44. N. Terrando, C. Monaco, D. Ma, B.M. Foxwell, M. Feldmann, and M. Maze Tumor necrosis factor-alpha triggers a cytokine cascade yielding postoperative cognitive decline Proc. Natl. Acad. Sci. USA 107 2010 20518 20522
45. G.C. Tombaugh, W.B. Rowe, A.R. Chow, T.H. Michael, and G.M. Rose Theta-frequency synaptic potentiation in CA1 in vitro distinguishes cognitively impaired from unimpaired aged Fischer 344 rats J. Neurosci. 22 2002 9932 9940
46. N. Toni, E.M. Teng, E.A. Bushong, J.B. Aimone, C. Zhao, A. Consiglio, H. van Praag, M.E. Martone, M.H. Ellisman, and F.H. Gage Synapse formation on neurons born in the adult hippocampus Nat. Neurosci. 10 2007 727 734
47. F. Van Hauwermeiren, R.E. Vandenbroucke, and C. Libert Treatment of TNF mediated diseases by selective inhibition of soluble TNF or TNFR1 Cytokine Growth Factor Rev. 22 2011 311 319
48. P. Victoratos, J. Lagnel, S. Tzima, M.B. Alimzhanov, K. Rajewsky, M. Pasparakis, and G. Kollias FDC-specific functions of p55TNFR and IKK2 in the development of FDC networks and of antibody responses Immunity 24 2006 65 77
49. S. Wang, S. Ota, B. Guo, J. Ryu, C. Rhodes, Y. Xiong, S. Kalim, L. Zeng, Y. Chen, M.A. Teitell, and X. Zhang Subcellular resolution mapping of endogenous cytokine secretion by nano-plasmonic-resonator sensor array Nano Lett. 11 2011 3431 3434
50. Z.Z. Xu, L. Zhang, T. Liu, J.Y. Park, T. Berta, R. Yang, C.N. Serhan, and R.R. Ji Resolvins RvE1 and RvD1 attenuate inflammatory pain via central and peripheral actions Nat. Med. 16 2010 592 597
51. G. Yang, C.N. Parkhurst, S. Hayes, and W.B. Gan Peripheral elevation of TNF-α leads to early synaptic abnormalities in the mouse somatosensory cortex in experimental autoimmune encephalomyelitis Proc. Natl. Acad. Sci. USA 110 2013 10306 10311
52. R. Yirmiya, and I. Goshen Immune modulation of learning, memory, neural plasticity and neurogenesis Brain Behav. Immun. 25 2011 181 213