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Modulating effect of cytokines on mechanisms of synaptic plasticity in the brain

Biochemistry (Moscow) volume 82, pages 264–274 (2017)Cite this article

Abstract

After accumulation of data showing that resident brain cells (neurons, astrocytes, and microglia) produce mediators of the immune system, such as cytokines and their receptors under normal physiological conditions, a critical need emerged for investigating the role of these mediators in cognitive processes. The major problem for understanding the functional role of cytokines in the mechanisms of synaptic plasticity, de novo neurogenesis, and learning and memory is the small number of investigated cytokines. Existing concepts are based on data from just three proinflammatory cytokines: interleukin-1 beta, interleukin-6, and tumor necrosis factor-alpha. The amount of information in the literature on the functional role of antiinflammatory cytokines in the mechanisms of synaptic plasticity and cognitive functions of mature mammalian brain is dismally low. However, they are of principle importance for understanding the mechanisms of local information processing in the brain, since they modulate the activity of individual cells and local neural networks, being able to reconstruct the processes of synaptic plasticity and intercellular communication, in general, depending on the local ratio of the levels of different cytokines in certain areas of the brain. Understanding the functional role of cytokines in cellular mechanisms of information processing and storage in the brain would allow developing preventive and therapeutic means for the treatment of neuropathologies related to impairment of these mechanisms.

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Abbreviations

AMPA:

α-amino-3-hydroxy-5-methyl-4-isoxazole

BDNF:

brain-derived neurotrophic factor

CaMKII:

Ca2+/calmodulin-dependent protein kinase II

CNS:

central nervous system

CREB:

cAMP response element-binding protein

Erk/MAPK:

signaling pathway

GABA:

γ-aminobutyric acid

GluA1 and GluA2:

subunits of AMPA receptors

IKK:

IκΒ kinase complex

IL-1:

interleukin-1

IL-1ra:

interleukin-1 receptor antagonist

IL-1RI and IL-1RII:

interleukin-1 receptors

IL6:

interleukin-6

JAK/STAT:

JAK kinase and signal transducers and activators of transcription

LSD:

long-term synaptic depression

LSP:

long-term synaptic potentiation

MHC-1:

major histocompatibility complex I

NF-κB:

nuclear factor kappa B

NMDA receptors:

N-methyl-D-aspartate receptors

Rab3:

small GTP-binding protein

RhoA:

small G-proteins

RIM proteins:

Rab3-interacting molecules

SB431542 :

inhibitor of TGFβ

TGFβ:

transforming growth factor beta

TNF:

tumor necrosis factor

TNFR1 and TNFR2:

TNF receptors

TTX:

tetrodotoxin

References

  1. Breder, C., Dinarello, C., and Saper, C. (1998) Interleukin-1 immunoreactive innervation of the human hypothalamus, Science, 240, 321–324.

    Article  Google Scholar 

  2. Plata-Salaman, C. R., Oomura, Y., and Kai, Y. (1988) Tumor necrosis factor and interleukin-1 beta: suppression of food intake by direct action in the central nervous system, Brain Res., 448, 106–114.

    CAS  Article  PubMed  Google Scholar 

  3. Stepanichev, M. Yu. (2005) Cytokines as neuromodulators in the central nervous system, Neurochemistry, 22, 5–11.

    Google Scholar 

  4. Vitkovic, L., Bockaert, J., and Jacque, C. (2000) “Inflammatory” cytokines: neuromodulators in normal brain? J. Neurochem., 74, 457–471.

    CAS  Article  PubMed  Google Scholar 

  5. Allan, S. M., and Rothwell, N. J. (2001) Cytokines and acute neurodegeneration, Nature Neurosci., 2, 734–744.

    CAS  Article  Google Scholar 

  6. Konsman, J. P., Parnet, P., and Dantzer, R. (2002) Cytokine-induced sickness behavior: mechanisms and implications, Trends Neurosci., 25, 154–159.

    CAS  Article  PubMed  Google Scholar 

  7. Wrona, D. (2006) Neural–immune interactions: an integrative view of the bidirectional relationship between the brain and immune systems, J. Neuroimmunol., 172, 38–58.

    CAS  Article  PubMed  Google Scholar 

  8. Turrigiano, G. G. (1999) Homeostatic plasticity in neuronal networks: the more things change, the more they stay the same, Trends Neurosci., 22, 221–227.

    CAS  Article  PubMed  Google Scholar 

  9. Malenka, R. C., and Nicoll, R. A. (1999) Long-term potentiation–a decade of progress? Science, 285, 1870–1874.

    CAS  Article  PubMed  Google Scholar 

  10. Vitureira, N., and Goda, Y. (2013) The interplay between Hebbian and homeostatic synaptic plasticity, J. Cell Biol., 203, 175–186.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. McAfoose, J., and Baune, B. T. (2009) Evidence for a cytokine model of cognitive function, Neurosci. Biobehav. Rev., 33, 355–366.

    CAS  Article  PubMed  Google Scholar 

  12. Hebb, D. O. (1949) Organization of Behavior: A Neuropsychological Theory (Weig, J., ed.) N. Y.

  13. Bliss, T. V. P., and Lynch, M. A. (1988) Long-Term Potentiation of Synaptic Transmission in the Hippocampus: Properties and Mechanisms in Long-Term Potentiation: from Biophysics to Behavior (Landfield, P. W., and Deadwyler, S. A., eds.) Liss, N. Y., pp. 3–72.

  14. Godukhin A. V., and Shchipakina, T. G. (1995) Mechanisms of synaptic plasticity: the role of phosphorylation of synaptic proteins and gene expression, Adv. Physiol. Sci., 26, 41–56.

    CAS  Google Scholar 

  15. Citri, A., and Malenka, R. C. (2008) Synaptic plasticity: multiple forms, functions, and mechanisms, Neuropsychopharmacol. Rev., 33, 18–41.

    Article  Google Scholar 

  16. Collingridge, G. L., Isaac, J. T., and Wang, Y. T. (2004) Receptor trafficking and synaptic plasticity, Nat. Rev. Neurosci., 5, 952–962.

    CAS  Article  PubMed  Google Scholar 

  17. Malenka, R. C., and Bear, M. F. (2004) LTP and LTD: an embarrassment of riches, Neuron, 44, 5–21.

    CAS  Article  PubMed  Google Scholar 

  18. Cingolani, L. A., and Goda, Y. (2008) Differential involvement of β3 integrin in pre- and postsynaptic forms of adaptation to chronic activity deprivation, Neuron Glia Biol., 4, 179–187.

    Article  PubMed  Google Scholar 

  19. Murphy, T. H., and Corbett, D. (2009) Plasticity during stroke recovery: from synapse to behavior, Nat. Rev. Neurosci., 10, 861–872.

    CAS  Article  PubMed  Google Scholar 

  20. Greer, P. L., and Greenberg, M. E. (2008) From synapse to nucleus: calcium-dependent gene transcription in the control of synapse development and function, Neuron, 59, 846–860.

    CAS  Article  PubMed  Google Scholar 

  21. West, A. E., and Greenberg, M. E. (2011) Neuronal activity-regulated gene transcription in synapse development and cognitive function, Cold Spring Harbor Perspect. Biol., 3.

    Google Scholar 

  22. Wood, M. A., Attner, M., Oliveira, A. M., Brindle, P. K., and Abel, T. (2006) A transcription factor-binding domain of the coactivator CBP is essential for long-term memory and the expression of specific target genes, Learn. Memory, 13, 609–617.

    CAS  Article  Google Scholar 

  23. Miller, P., Zhabotinsky, A. M., Lisman, J. E., and Wang, X. J. (2005) The stability of a stochastic CaMKII switch: dependence on the number of enzyme molecules and protein turnover, PLoS Biol., 3, 107.

    Article  Google Scholar 

  24. Casar, B., Pinto, A., and Crespo, P. (2008). Essential role of ERK dimers in the activation of cytoplasmic but not nuclear substrates by ERK-scaffold complexes, Mol. Cell, 31, 708–721.

    CAS  Article  PubMed  Google Scholar 

  25. Sajikumar, S., Navakkode, S., and Frey, J. U. (2005) Protein synthesis-dependent long-term functional plasticity: methods and techniques, Curr. Opin. Neurobiol., 15, 607–613.

    CAS  Article  PubMed  Google Scholar 

  26. Lscher, C., and Malenka, R. C. (2012) NMDA ReceptorDependent Long-Term Potentiation and Long-Term Depression (LTP/LTD), Cold Spring Harbor Laboratory Press, N. Y., pp. 1–10.

    Google Scholar 

  27. Raymond, C. R. (2007) LTP forms 1, 2 and 3: different mechanisms for the “long” in long-term potentiation, Trends Neurosci., 30, 168–175.

    Article  Google Scholar 

  28. Spedding, M., and Gressens, P. (2008) Neurotrophins and cytokines in neuronal plasticity, Novartis Found Symp., 28, 222–233.

    Article  Google Scholar 

  29. McClung, C. A., and Nestler, E. J. (2008) Neuroplasticity mediated by altered gene expression, Neuropsychopharmacology, 33, 3–17.

    CAS  Article  PubMed  Google Scholar 

  30. Pozo, K., and Goda, Y. (2010) Unraveling mechanisms of homeostatic synaptic plasticity, Neuron, 66, 337–351.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  31. Turrigiano, G. (2008) Homeostatic synaptic plasticity, in Structural and Functional Organization of the Synapse (Hell, J. W., and Ehlers, M. D., eds.) Springer Science, N. Y., pp. 535–548.

    Chapter  Google Scholar 

  32. Echegoyen, J., Neu, A., Graber, K. D., and Soltesz, I. (2007) Homeostatic plasticity studied using in vivo hippocampal activity-blockade: synaptic scaling, intrinsic plasticity and age-dependence, PLoS One, 2, e700.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Bartley, A. F., Huang, Z. J., Huber, K. M., and Gibson, J. R. (2008) Differential activity-dependent, homeostatic plasticity of two neocortical inhibitory circuits, J. Neurophysiol., 100, 1983–1994.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Yu, W., Morishita, W., Tsui, J., Gaietta, G., Deerinck, T. J., Adams, S. R., Garner, C. C., Tsien, R. Y., Ellisman, M. H., and Malenka, R. C. (2004) Activity-dependent regulation of dendritic synthesis and trafficking of AMPA receptors, Nat. Neurosci., 7, 244–253.

    Article  Google Scholar 

  35. Sutton, M. A., Ito, H. T., Cressy, P., Kempf, C., Woo, J. C., and Schuman, E. M. (2006) Miniature neurotransmission stabilizes synaptic function via tonic suppression of local dendritic protein synthesis, Cell, 125, 785–799.

    CAS  Article  PubMed  Google Scholar 

  36. Rabinowitch, I., and Segev, I. (2008) Two opposing plasticity mechanisms pulling a single synapse, Trends Neurosci., 31, 377–383.

    CAS  Article  PubMed  Google Scholar 

  37. Lee, K. J., Park, T. S., Kim, H., Greenough, W. T., Pak, D. T., and Rhyn, I. J. (2013) Motor skill training induces coordinated strengthening and weakening between neighboring synapses, J. Neurosci., 33, 9794–9799.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  38. Arendt, K. L., Sarti, F., and Chen, L. (2013) Chronic inactivation of a neural circuit enhances LTP by inducing silent synapse formation, J. Neurosci., 33, 2087–2096.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  39. Goshen, I., and Yirmia, R. (2007) The role of pro-inflammatory cytokines in memory processes and neural plasticity, Psychoneuroimmunology, 1, 337–367.

    Article  Google Scholar 

  40. Pribiag, H., and Stellwagen, D. (2014) Neuroimmune regulation of homeostatic synaptic plasticity, Neuropharmacology, 78, 13–22.

    CAS  Article  PubMed  Google Scholar 

  41. Yirmiya, R., and Goshen, I. (2011) Immune modulation of learning, memory, neural plasticity and neurogenesis, Brain Behav. Immun., 25, 181–213.

    CAS  Article  PubMed  Google Scholar 

  42. Donna, L., and Gruol, C. (2015) IL-6 regulation of synaptic function in the CNS, Neuropharmacology, 96, 42–54.

    Article  Google Scholar 

  43. Tancredi, V., D’Antuono, M., Cafe, C., Giovedi, S., Bue, M. C., D’Arcangelo, G., Onofri, F., and Benfenati, F. (2000) The inhibitory effects of interleukin-6 on synaptic plasticity in the rat hippocampus are associated with an inhibition of mitogen-activated protein kinase ERK, J. Neurochem., 75, 634–643.

    CAS  Article  PubMed  Google Scholar 

  44. Beattle, T. C., Stellwagen, D., Morishita, W., Bresnahan, J. C., Ha, B. K., Von Zastrow, M., Beattle, M. S., and Malenka, R. C. (2002) Control of synaptic strength by glial TNF alpha, Science, 295, 2282–2285.

    Article  Google Scholar 

  45. Stellwagen, D., Beattie, E. C., Seo, J. Y., and Malenka, R. C. (2005) Differential regulation of AMPA receptor and GABA receptor trafficking by tumor necrosis factor-alpha, J. Neurosci., 25, 3219–3228.

    CAS  Article  PubMed  Google Scholar 

  46. Grilli, M., Barbieri, I., Basudev, H., Brusa, R., Casati, C., Lozza, G., and Ongini, E. (2000) Interleukin-10 modulates neuronal threshold of vulnerability to ischaemic damage, Eur. J. Neurosci., 12, 2265–2272.

    CAS  Article  PubMed  Google Scholar 

  47. Molina-Holgado, E., Vela, J. M., Arevalo-Martin, A., and Guaza, C. (2001) LPS/IFN-gamma cytotoxicity in oligodendroglial cells: role of nitric oxide and protection by the antiinflammatory cytokine IL-10, Eur. J. Neurosci., 13, 493–502.

    CAS  Article  PubMed  Google Scholar 

  48. Krieglstein, K., Zheng, F., Unsicker, K., and Alzheimer, C. (2011) More than being protective: functional roles for TGF/activin signaling pathways at central synapses, Trends Neurosci., 34, 421–429.

    CAS  Article  PubMed  Google Scholar 

  49. Yu, C. Y., Gui, W., He, H. Y., Wang, X. S., Zuo, J., Huang, L., Zhou, N., Wang, K., and Wang, Y. (2014) Neuronal and astroglial TGFβ-Smad3 signaling pathways differentially regulate dendrite growth and synaptogenesis, Neuronal Med., 16, 457–472.

    CAS  Google Scholar 

  50. Caraci, F., Gulisano, W., Guida, C. A., Impellizzeri, A. A., Drago, F., Puzzo, D., and Palmeri, A. (2015) A key role for TGF-β1 in hippocampal synaptic plasticity and memory, Sci. Rep., 5, 1–10.

    Article  Google Scholar 

  51. Nicolas, C. S., Peineau, S., Amici, M., Csaba, Z., Fatouri, A., Javalet, C., Colett, V. J., Hilderbrandt, L., Seaton, G., Choi, S. L., Sim, S. E., Bradley, C., Lee, K., Zhuo, M., Kaang, B. K., Gressens, P., Dournaud, P., Fitzjohn, S. M., Bortolotto, Z. A., Cho, K., and Collingridge, G. L. (2012) The JAK/STAT pathway is involved in synaptic plasticity, Neuron, 73, 374–390.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  52. Copf, T., Goguel, V., Lampin- Saint-Amaux, A., Scaplehorn, N., and Preat, T. (2011) Cytokine signaling through the JAK/STAT pathway is required for long-term memory in Drosophila, PNAS, 108, 8059–8064.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  53. Rothwell, N. J., and Luheshi, G. N. (2000) Interleukin I in the brain: biology, pathology and therapeutic target, Trends Neurosci., 23, 618–625.

    CAS  Article  PubMed  Google Scholar 

  54. Thornberry, N. A., Bull, H. G., Calaycay, J. R., Chapman, K. T., Howard, A. D., Kosture, M. J., Miller, D. K., Molineaux, S. M., Weidner, J. R., Aunins, J., Elliston, K. O., Avala, J. M., Casano, F. J., Chin, J., Ding, G. J. F., Egger, L. A., Gaffney, E. P., Limjnco, G., Palyha, O. C., Rajn, S. M., Rolando, A. M., Salley, J. P., Yamin, T. T., Lee, T. D., Shivelly, J. E., Maccross, M., Mumford, R. A., Schmidt, J. A., and Tocci, M. J. (1992) A novel heterodimeric cysteine protease is required for interleukin-1β processing in monocytes, Nature, 356, 768–774.

    CAS  Article  PubMed  Google Scholar 

  55. Rothwell, N. J. (1991) Functions and mechanisms of interleukin-1 in the brain, Trends Pharm. Sci., 12, 430–436.

    CAS  Article  PubMed  Google Scholar 

  56. Di Donato, J. A., Nayakawa, M., Rothware, D. M., Zandi, E., and Karin, M. (1997) A cytokine-responsive IkB kinase that activates the transcription factor NF-κB, Nature, 388, 548–554.

    Article  Google Scholar 

  57. O’Neill, L. A., and Greene, C. (1998) Signal transduction pathways activated by the IL-1 receptor family: ancient signaling machinery in mammals, insects, and plants, J. Leukocyte Biol., 63, 650–657.

    PubMed  Google Scholar 

  58. Turnbull, A. V., and Rivier, C. L. (1999) Regulation of the hypothalamic–pituitary–adrenal axis by cytokines: actions and mechanisms of action, Physiol. Rev., 79, 1–71.

    CAS  PubMed  Google Scholar 

  59. Kluger, M. J., Kozak, W., Leon, L. R., Soszynski, D., and Conn, C. A. (1998) Fever and antipyresis, Prog. Brain Res., 115, 465–475.

    CAS  Article  PubMed  Google Scholar 

  60. Krueger, J. M., Fang, J., Taishi, P., Chen, Z., Kushikata, T., and Gardi, J. (1998) Sleep: a physiologic role for IL-1 beta and TNF-alpha, Ann. N. Y. Acad. Sci., 856, 148–159.

    CAS  Article  PubMed  Google Scholar 

  61. Diana, A., Van Dam, A. M., Winblad, B., and Schultzberg, M. (1999) Co-localization of interleukin-1 receptor type I and interleukin-1 receptor antagonist with vasopressin in magnocellular neurons of the paraventricular and supraoptic nuclei of the rat hypothalamus, Neuroscience, 89, 137–147.

    CAS  Article  PubMed  Google Scholar 

  62. Pringle, A. K., Gardner, C. R., and Walker, R. J. (1996) Reduction of cerebellar GABAA responses by interleukin-1 (IL-1) through an indometacin insensitive mechanism, Neuropharmacology, 35, 147–152.

    CAS  Article  PubMed  Google Scholar 

  63. Cunningham, A. J., Murray, C. A., O’Neill, L. A. J., Lynch, M. A., and O’Connor, J. J. (1996) Interleukin-1β (IL-1β) and tumor necrosis factor (TNF) inhibit long-term potentiation in the rat dentate gyrus in vitro, Neurosci. Lett., 203, 17–20.

    CAS  Article  PubMed  Google Scholar 

  64. Zhou, C., Ye, H. H., Wang, S. Q., and Chai, Z. (2006) Interleukin-1β regulation of N-type Ca2+ channels in cortical neurons, Neurosci. Lett., 403, 181–185.

    CAS  Article  PubMed  Google Scholar 

  65. Wang, C. X., and Shuaib, A. (2002) Involvement of inflammatory cytokines in central nervous system injury, Prog. Neurobiol., 67, 161–172.

    CAS  Article  PubMed  Google Scholar 

  66. Miller, L. G., Galpern, W. R., Dunlap, K., Dinarello, C. A., and Turner, T. J. (1991) Interleukin-1 augments gamma-aminobutyric acid A receptor function in brain, Mol. Pharmacol., 39, 105–108.

    CAS  PubMed  Google Scholar 

  67. Plata-Salaman, C. R., and Ffrench-Mullen, J. M. (1992) Interleukin-1 beta depresses calcium currents in CA1 hippocampal neurons at pathophysiological concentrations, Brain Res., 29, 221–223.

    CAS  Google Scholar 

  68. Viviani, B., Gardoni, F., and Marinovich, M. (2007) Cytokines and neuronal ion channels in health and disease, Inter. Rev. Neurobiol., 82, 247–263.

    CAS  Article  Google Scholar 

  69. Fenster, C. P., Fenster, S. D., Leahy, H. P., Kurschner, C., and Blundon, J. A. (2007) Modulation Kv4.2 K+ currents by neuronal interleukin-16, a PDZ domain-containing protein expressed in the hippocampus and cerebellum, Brain Res., 1162, 19–31.

    CAS  Article  PubMed  Google Scholar 

  70. Liu, Z., Fang, X. X., Chen, Y. P., Qiu, Y. H., and Peng, Y. P. (2013) Interleukin-6 prevents NMDA-induced neuronal Ca2+ overload via suppression of IP3 receptors, Brain Injury, 27, 1047–1055.

    Article  PubMed  Google Scholar 

  71. Floyd, R., and Krueger, J. (1997) Diurnal variation of TNF alpha in the rat brain, Neuroreport, 8, 915–918.

    CAS  Article  PubMed  Google Scholar 

  72. Szelenyl, J. (2001) Cytokines and the central nervous system, Brain Res. Bull., 54, 329–338.

    Article  Google Scholar 

  73. Kinouchi, K., Brown, G., Pasternak, G., and Donner, D. (1991) Identification and characterization of receptors for tumor necrosis factor alpha in the brain, Biochem. Biophys. Res. Commun., 181, 1532–1538.

    CAS  Article  PubMed  Google Scholar 

  74. MacEwan, D. J. (2002) TNF receptor subtype signaling: differences and cellular consequences, Cell Signal., 14, 477–492.

    CAS  Article  PubMed  Google Scholar 

  75. Furuno, T., and Nakanishi, M. (2006) Neurotrophic factors and tumor necrosis factor-α induced translocation of NF-κB in rat PC12 cells, Neurosci. Lett., 392, 240–244.

    CAS  Article  PubMed  Google Scholar 

  76. Eder, J. (1997) Tumor necrosis factor alpha and interleukin 1 signaling: do MAPKK kinases connect it all? Trends Pharmacol. Sci., 18, 319–322.

    CAS  Article  PubMed  Google Scholar 

  77. Houzen, H., Kikuchi, S., Kanno, M., Shinpo, K., and Tashiro, K. (1997) Tumor necrosis factor enhancement of transient outward potassium currents in cultured rat cortical neurons, J. Neurosci. Res., 50, 990–999.

    CAS  Article  PubMed  Google Scholar 

  78. Furukawa, K., and Mattson, M. P. (1998) The transcription factor NF-κB mediates increases in calcium currents and decreases in NMDAand AMPA/kainite-induced currents induced by tumor necrosis factor-α in hippocampal neurons, J. Neurochem., 70, 1876–1886.

    CAS  Article  PubMed  Google Scholar 

  79. Vezzani, A., and Viviani, B. (2015) Neuromodulatory properties of inflammatory cytokines and their impact on neuronal excitability, Neuropharmacology, 96, 70–82.

    CAS  Article  PubMed  Google Scholar 

  80. Strle, K., Zhou, J. H., Shen, W. H., Broussard, S. R., Johnson, R. W., Freund, G. G., Dantzer, R., and Kelly, K. W. (2001) Interleukin-10 in the brain, Crit. Rev. Immunol., 21, 427–449.

    CAS  Article  PubMed  Google Scholar 

  81. Beattie, M. S., Harrington, A. W., Lee, R., Kim, J. Y., Boyce, S. L., Longo, F. M., Bresnahan, J. C., Hempstead, B. L., and Yoon, S. O. (2002) ProNGF induces p75-mediated death of oligodendrocytes following spinal cord injury, Neuron, 36, 375–386.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  82. Schafers, M., and Sorkin, L. (2008) Effects of cytokines on neuronal excitability, Neurosci. Lett., 437, 188–193.

    Article  PubMed  Google Scholar 

  83. Levin, S. G., and Godukhin, O. V. (2011) Anti-inflammatory cytokines, TGF-β1 and IL-10, exert anti-hypoxic action and abolish posthypoxic hyperexcitability in hippocampal slice neurons: comparative aspects, Exp. Neurol., 232, 329–332.

    CAS  Article  PubMed  Google Scholar 

  84. Turovskaya, M. V., Turovsky, E. A., Zinchenko, V. P., Levin, S. G., and Godukhin, O. V. (2012) Interleukin-10 modulates [Ca2+]i response induced by repeated NMDA receptor activation with brief hypoxia through inhibition of InsP3-sensitive internal stores in hippocampal neurons, Neurosci. Lett., 516, 151–155.

    CAS  Article  PubMed  Google Scholar 

  85. Savina, T. A., Shchipakina, T. G., Levin, S. G., and Godukhin, O. V. (2013) Interleukin-10 prevents the hypoxia-induced decreases in expressions of AMPA receptor subunit GluA1 and alpha subunit of Ca2+/calmodulindependent protein kinase II in hippocampal neurons, Neurosci. Lett., 534, 279–284.

    CAS  Article  PubMed  Google Scholar 

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  1. Institute of Theoretical and Experimental Biophysics, Russian Academy of Sciences, 142290, Pushchino, Moscow Region, Russia

    S. G. Levin & O. V. Godukhin

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Published in Russian in Biokhimiya, 2017, Vol. 82, No. 3, pp. 397-409.

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Levin, S.G., Godukhin, O.V. Modulating effect of cytokines on mechanisms of synaptic plasticity in the brain. Biochemistry Moscow 82, 264–274 (2017). https://doi.org/10.1134/S000629791703004X

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Keywords

  • cytokines
  • synaptic plasticity
  • interleukin-1 beta
  • tumor necrosis factor-alpha
  • interleukin-6
  • interleukin-10
  • transforming growth factor