Механизмы кальций-зависимой десенситизации NMDA рецепторов

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Работа выполнена в рамках государственного задания № АААА-А18-118012290427-7.

Список литературы

1. Pina-Crespo, J.C., and Gibb, A.J. (2002) Subtypes of NMDA receptors in new-born rat hippocampal granule cells, J. Physiol., 541, 41–64.

2. Hansen, K.B., Ogden, K.K., Yuan, H., and Traynelis, S.F. (2014) Distinct functional and pharmacological properties of triheteromeric GluN1/GluN2A/GluN2B NMDA receptors, Neuron, 81, 1084–1096.

3. Sibarov, D.A., Stepanenko, Y.D., Silantiev, I.V., Abushik, P.A., Karelina, T.V., and Antonov, S.M. (2018) Developmental changes of synaptic and extrasynaptic NMDA receptor expression in rat cerebellar neurons in vitro, J. Mol. Neurosci., 64, 300–311.

4. Dingledine, R., Borges, K., Bowie, D., and Traynelis, S.F. (1999) The glutamate receptor ion channels, Pharmacol. Rev., 51, 7–61.

5. Glasgow, N.G., Siegler Retchless, B., and Johnson, J.W. (2015) Molecular bases of NMDA receptor subtype-dependent properties, J. Physiol., 593, 83–95.

6. Kleckner, N.W., and Dingledine, R. (1988) Requirement for glycine in activation of NMDA-receptors expressed in Xenopus oocytes, Science, 241, 835–837.

7. Wolosker, H., Blackshaw, S., and Snyder, S.H. (1999) Serine racemase: a glial enzyme synthesizing D-serine to regulate glutamate-N-methyl-D-aspartate neurotransmission, Proc. Natl. Acad. Sci. USA, 96, 13409–13414.

8. Patneau, D.K., and Mayer, M.L. (1990) Structure-activity relationships for amino acid transmitter candidates acting at N-methyl-D-aspartate and quisqualate receptors, J. Neuro-sci., 10, 2385–2399.

9. Zarei, M.M., and Dani, J.A. (1994) Ionic permeability characteristics of the N-methyl-D-aspartate receptor channel, J. Gen. Physiol., 103, 231–248.

10. Bliss, T.V.P., and Collingridge, G.L. (1993) A synaptic model of memory: long-term potentiation in the hippocampus, Nature, 361, 31–39.

11. Bear, M.F. (1995) Mechanism for a sliding synaptic modification threshold, Neuron, 15, 1–4.

12. Lisman, J., Schulman, H., and Cline, H. (2002) The molecular basis of CaMKII function in synaptic and behavioural memory, Nat. Rev. Neurosci., 3, 175–190.

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

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

15. Citri, A., and Malenka, R.C. (2007) Synaptic plasticity: multiple forms, functions, and mechanisms, Neuropsychopharmacology, 33, 18–41.

16. Dore, K., Aow, J., and Malinow, R. (2016) The emergence of NMDA receptor metabotropic function: insights from imaging, Front. Synapt. Neurosci., 8, 1–9.

17. Choi, D.W. (1995) Calcium: still center-stage in hypoxicischemic neuronal death, Trends Neurosci., 18, 58–60.

18. Paoletti, P., Bellone, C., and Zhou, Q. (2013) NMDA receptor subunit diversity: impact on receptor properties, synaptic plasticity and disease, Nat. Rev. Neurosci., 14, 383–400.

19. Mayer, M.L., and Armstrong, N. (2004) Structure and function of glutamate receptor ion channels, Annu. Rev. Physiol., 66, 161–181.

20. Mayer, M.L., Vyklicky, L., and Westbrook G.L. (1989) Modulation of excitatory amino acid receptors by group IIB metal cations in cultured mouse hippocampal neurons, J. Physiol., 415, 329–350.

21. McBain, C.J., and Mayer, M.L. (1994) N-methyl-D-aspartic acid receptor structure and function, Physiol. Rev., 74, 723–760.

22. Kutsuwada, T., Kashiwabuchi, N., Mori, H., Sakimura, K., Kushiya, E., Araki, K., Meguro, H., Masaki, H., Kumanishi, T., Arakawa, M., and Mishina, M. (1992) Molecular diversity of the NMDA receptor channel, Nature, 358, 36–41.

23. Ishii, T., Moriyoshi, K., Sugihara, H., Sakurada, K., Kadotani, H., Yokoi, M., Akazawa, C., Shigemoto, R., Mizuno, N., Masu, M, and Nakanishi, S. (1993) Molecular characterization of the family of the N-methyl-D-aspartate receptor subunits, J. Biol. Chem., 268, 2836–2843.

24. Clark, G.D., Clifford, D.B., and Zorumski, C.F. (1990) The effect of agonist concentration, membrane voltage and calcium on N-methyl-D-aspartate receptor desensitization, Neuroscience, 39, 787–797.

25. Legendre, P., Rosenmund, C., and Westbrook, G.L. (1993) Inactivation of NMDA channels on hippocampal neurons by intracellular calcium, J. Neurosci., 13, 674–684.

26. Rosenmund, C., and Westbrook, G.L. (1993) Calcium-induced actin depolymerization reduces NMDA channel activity, Neuron, 10, 805–814.

27. Vyklicky, L.J. (1993) Calcium-mediated modulation of N-methyl-D-aspartate (NMDA) responses in cultured rat hippocampal neurons, J. Physiol. (London), 470, 575–600.

28. Traynelis, S.F., Wollmuth, L.P., McBain, C.J., Menniti, F.S., Vance, K.M., Ogden, K.K., Hansen, K.B., Yuan, H., Myers, S.J., and Dingledine, R. (2010) Glutamate receptor ion channels: structure, regulation, and function, Pharm. Rev., 62, 405–496.

29. Hedegaard, M., Hansen, K.B., Andersen, K.T., Brauner-Osborne, H., and Traynelis, S.F. (2012) Molecular pharmacology of human NMDA receptors, Neurochem. Int., 61, 601–609.

30. Dravid, S.M., Erreger, K., Yuan, H., Nicholson, K., Le, P., Lyuboslavsky, P., Almonte, A., Murray, E., Mosely, C., Barber, J., French, A., Balster, R., Murray, T.F., and Traynelis, S.F. (2007) Subunit-specific mechanisms and proton sensitivity of NMDA receptor channel block, J. Physiol., 581, 107–128.

31. Wyllie, D.J., Behe, P., and Colquhoun, D. (1998) Single-channel activations and concentration jumps: comparison of recombinant NR1a/NR2A and NR1a/NR2D NMDA receptors, J. Physiol., 510, 1–18.

32. Vicini, S., Wang, J.F., Li, J.H., Zhu, W.J., Wang, Y.H., Luo, J.A.H., Wolfe, B.B., and Grayson, D.R. (1998) Functional and pharmacological differences between recombinant N-methyl-D-aspartate receptors, J. Neurophysiol., 79, 555–566.

33. Hansen, K.B., and Traynelis, S.F. (2011) Structural and mechanistic determinants of a novel site for noncompetitive inhibition of GluN2D-containing NMDA receptors, J. Neurosci., 31, 3650–3661.

34. Burnashev, N., Schoepfer, R., Monyer, H., Ruppersberg, J.P., Gunther., W., Seeburg, P.H., and Sakmann, B. (1992) Сontrol by asparagine residues of calcium permeability and magnesium blockade in the NMDA receptor, Science, 257, 1415–1419.

35. Pankratov, Y., and Lalo, U. (2014) Calcium permeability of ligand-gated Ca(2+) channels, Eur. J. Pharmacol., 739C, 60–73.

36. Krupp, J.J., Vissel, B., Thomas, C.G., Heinemann, S.F., and Westbrook, G.L. (1999) Interactions of calmodulin and alpha-actinin with the NR1 subunit modulate Ca2+- dependent inactivation of NMDA receptors, J. Neurosci., 19, 1165–1178.

37. Medina, I., Filippova, N., Charton, G., Rougeole, S., Ben-Ari, Y., Khrestchatisky, M., and Bregestovski, P. (1995) Calcium-dependent inactivation of heteromeric NMDA receptor-channels expressed in human embryonic kidney cells, J. Physiol., 482, 567–573.

38. Hardingham, G.E., and Bading, H. (2010) Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders, Nat. Rev. Neurosci., 11, 682–696.

39. Schwartz, E.J., Rothman, J.S., Dugue, G.P., Diana, M., Rousseau, C., Silver, R.A., and Dieudonne, S. (2012) NMDA receptors with incomplete Mg2+ block enable low-frequency transmission through the cerebellar cortex, J. Neurosci., 32, 6878–6893.

40. Hildebrand, M. E., Pitcher, G. M., Harding, E. K., Li, H., Beggs, S., and Salter, M. W. (2014) GluN2B and GluN2D NMDARs dominate synaptic responses in the adult spinal cord, Sci. Rep., 4, 4094.

41. Lesca, G., Rudolf, G., Bruneau, N., Lozovaya, N., Labalme, A., Boutry-Kryza, N., Salmi, M., Tsintsadze, T., Addis, L., Motte, J., Wright, S., Tsintsadze, V., Michel, A., Doummar, D., Lascelles, K., Strug, L., Waters, P., de Bellescize, J., Vrielynck, P., de Saint Martin, A., Ville, D., Ryvlin, P., Arzimanoglou, A., Hirsch, E., Vincent, A., Pal, D., Burnashev, N., Sanlaville, D., and Szepetowski, P. (2013) GRIN2A mutations in acquired epileptic aphasia and related childhood focal epilepsies and encephalopathies with speech and language dysfunction, Nat. Genet., 45, 1061–1066.

42. Burnashev, N., and Szepetowski, P. (2015) NMDA receptor subunit mutations in neurodevelopmental disorders, Curr. Opin. Pharmacol., 20, 73–82.

43. Sibarov, D.A., Bruneau, N., Antonov, S.M., Szepetowski, P., Burnashev, N., and Giniatullin, R. (2017) Functional properties of human NMDA receptors associated with epilepsy-related mutations of GluN2A subunit, Front. Cell. Neurosci., 11, 155, doi:10.3389/fncel.2017.00155.

44. Mayer, M.L., and Westbrook, G.L. (1985) The action of N-methyl-D-aspartic acid on mouse spinal neurones in culture, J. Physiol., 361, 65–90.

45. Zorumski, C.F., Yang, J., and Fischbach, G.D. (1989) Calcium dependent, slow desensitization distinguishes different types of glutamate receptors, Cell. Mol. Neurobiol., 9, 95–104.

46. Babu, Y.S., Sack, J.S, Greenhough, T.J, Bugg, C.E., Means, A.R., and Cook, W.J. (1985) Three-dimensional structure of calmodulin, Nature, 315, 37–40.

47. Crivici, A., and Ikura, M. (1995) Molecular and structural basis of target recognition by calmodulin, Annu. Rev. Biophys. Biomol. Struct., 24, 85–116.

48. Yap, K.L., Ames, J.B., Swindells, M.B., and Ikura, M. (1999) Diversity of conformational states and changes within the EF-hand protein superfamily, Proteins, 37, 499–507.

49. Ehlers, M.D., Zhang, S., Bernhadt, J.P., and Huganir, R.L. (1996) Inactivation of NMDA receptors by direct interaction of calmodulin with the NR1 subunit, Cell, 84, 745–755.

50. Chen, T.Y., and Yau, K.W. (1994) Direct modulation by Ca2+-calmodulin of cyclic nucleotide-activated channel of rat olfactory receptor neurons, Nature, 368, 545–548.

51. Liu, M., Chen, T.Y., Ahamed, B., Li, J., and Yau, K.W. (1994) Calcium calmodulin modulation of the olfactory cyclic nucleotide–gated cation channel, Science, 266, 1348–1354.

52. Lee, A., Wong, S.T., Gallagher, D., Li, B., Storm, D.R., Scheuer, T., and Catterall, W.A. (1999) Ca2+/calmodulin binds to and modulates P/Q-type calcium channels, Nature, 399, 155–159.

53. Peterson, B.Z., Lee, J.S., Mulle, J.G., Wang, Y., de Leon, M., and Yue, D.T. (2000) Critical determinants of Ca2+-dependent inactivation within an EF-hand motif of L-type Ca2+ channels, Biophys. J., 78, 1906–1920.

54. Zuhlke, R.D., Pitt, G.S., Deisseroth, K., Tsien, R.W., and Reuter, H. (1999) Calmodulin supports both inactivation and facilitation of L-type calcium channels, Nature, 399, 159–162.

55. Thomas, C.G., Krupp, J.J., Bagley, E.E., Bauzon, R., Heinemann, S.F., Vissel, B., and Westbrook, G.L. (2006) Probing N-methyl-D-aspartate receptor desensitization with the substituted-cysteine accessibility method, Mol. Pharmacol., 69, 1296–1303.

56. Ogden, K.K., Chen, W., Swanger, S.A., McDaniel, M.J., Fan, L.Z., Hu, C., Tankovic, A., Kusumoto, H., Kosobucki, G.J., Schulien, A.J., Su, Z., Pecha, J., Bhattacharya, S., Petrovski, S., Cohen, A.E., Aizenman, E., Traynelis, S.F., and Yuan, H. (2017) Molecular mechanism of disease-associated mutations in the pre-M1 helix of NMDA receptors and potential rescue pharmacology, PLoS Genetics, 13, e1006536.

57. Zhang, S., Ehlers, M.D., Bernhardt, J.P., Su, C.T., and Huganir, R.L. (1998) Calmodulin mediates calcium-dependent inactivation of N-methyl-D-aspartate receptors, Neuron, 21, 443–453.

58. Vissel, B., Krupp, J.J., Heinemann, S.F., and Westbrook, G.L. (2002) Intracellular domains of NR2 alter calcium-dependent inactivation of N-methyl-D-aspartate receptors, Mol. Pharmacol., 61, 595–605.

59. Tingley, W.G., Roche, K.W., Thompson, A.K., and Huganir, R.L. (1993) Regulation of NMDA receptor phosphorylation by alternative splicing of the C-terminal domain, Nature, 364, 70–73.

60. Raymond, L.A., Tingley, W.G., Blackstone, C.D., Roche, K.W., and Huganir, R.L. (1994) Glutamate receptor modulation by protein phosphorylation, J. Physiol. Paris, 88, 181–192.

61. Ehlers, M.D., Tingley, W.G., and Huganir, R.L. (1995) Regulated subcellular distribution of the NR1 subunit of the NMDA receptor, Science, 269, 1734–1737.

62. Ehlers, M.D., Fung, E.T., O’brien, R.J., and Huganir, R.L. (1998) Splice variant-specific interaction of the NMDA receptor subunit NR1 with neuronal intermediate filaments, J. Neurosci., 18, 720–730.

63. Wyszynski, M., Kharazia, V., Shanghvi, R., Rao, A., Beggs, A.H., Craig, A.M., Weinberg, R., and Sheng, M. (1998) Differential regional expression and ultrastructural localization of alpha-actinin-2, a putative NMDA receptor-anchoring protein, in rat brain, J. Neurosci., 18, 1383–1392.

64. Allison, D.W., Gelfand, V.I., Spector, I., and Craig, A.M. (1998) Role of actin in anchoring postsynaptic receptors in cultured hippocampal neurons: differential attachment of NMDA versus AMPA receptors, J. Neurosci., 18, 2423–2436.

65. Villarroel, A., Regalado, M.P., and Lerma, J. (1998) Glycine-independent NMDA receptor desensitization: localization of structural determinants, Neuron, 20, 329–339.

66. Krupp, J.J., Vissel, B., Heinemann, S.F., and Westbrook, G.L. (1996) Calcium-dependent inactivation of recombinant N-methyl-D-aspartate receptors is NR2 subunit specific, Mol. Pharmacol., 50, 1680–1688.

67. Wyllie, D.J., Behe, P., and Colquhoun, D. (1998) Single-channel activations and concentration jumps: comparison of recombinant NR1a/NR2A and NR1a/NR2D NMDA receptors, J. Physiol. (London), 510, 1–18.

68. Stern-Bach, Y., Russo, S., Neuman, M., and Rosenmund, C. (1998) A point mutation in the glutamate binding site blocks desensitization of AMPA receptors, Neuron, 21, 907–918.

69. Rozov, A., and Burnashev, N. (2016) Fast interaction between AMPA and NMDA receptors by intracellular calcium, Cell Calcium, 60, 407–414.

70. Rycroft, B.K., and Gibb, A.J. (2004) Regulation of single NMDA receptor channel activity by alpha-actinin and calmodulin in rat hippocampal granule cells, J. Physiol., 557, 795–808.

71. Medina, I., Filippova, N., Barbin, G., Ben-Ari, Y., and Bregestovski, P. (1994) Kainate-induced inactivation of NMDA currents via an elevation of intracellular Ca2+ in hippocampal neurons, J. Neurophysiol., 72, 456–465.

72. Gibson, H.E., Edwards, J.G., Page, R.S., Van Hook, M.J., and Kauer, J.A. (2008) TRPV1 channels mediate longterm depression at synapses on hippocampal interneurons, Neuron, 57, 746–759.

73. Vyklicky, L., Novakova-Tousova, K., Benedikt, J., Samad, A., Touska, F., and Vlachova, V. (2008) Calcium-dependent desensitization of vanilloid receptor TRPV1: a mechanism possibly involved in analgesia induced by topical application of capsaicin, Physiol. Res., 57 Suppl. 3, S59–68.

74. Emptage, N., Bliss, T.V., and Fine, A. (1999) Single synaptic events evoke NMDA receptor-mediated release of calcium from internal stores in hippocampal dendritic spines, Neuron, 22, 115–124.

75. Kapur, A., Yeckel, M., and Johnston, D. (2001) Hippocampal mossy fiber activity evokes Ca2+ release in CA3 pyramidal neurons via a metabotropic glutamate receptor pathway, Neuroscience, 107, 59–69.

76. Goldberg, J. H., Yuste, R., and Tamas, G. (2003) Ca2+ imaging of mouse neocortical interneurone dendrites: contribution of Ca2+-permeable AMPA and NMDA receptors to subthreshold Ca2+ dynamics, J. Physiol., 551, 67–78.

77. Kim, M.-H., Lee, S.-H., Park, K. H., Ho, W.-K., and Lee, S.-H. (2003) Distribution of K+-dependent Na+/Ca2+ exchangers in the rat supraoptic magnocellular neuron is polarized to axon terminals, J. Neurosci., 23, 11673–11680.

78. Komori, Y., Tanaka, M., Kuba, M., Ishii, M., Abe, M., Kitamura, N., Verkhratsky, A., Shibuya, I., and Dayanithi, G. (2010) Ca2+ homeostasis, Ca2+ signalling and somatodendritic vasopressin release in adult rat supraoptic nucleus neurones, Cell Calcium, 48, 324–332.

79. Carafoli, E., Santella, L., Branca, D., and Brini, M. (2001) Generation, control, and processing of cellular calcium signals, Crit. Rev. Biochem. Mol. Biol., 36, 107–260.

80. Hilgemann, D.W. (1990) Regulation and deregulation of cardiac Na+-Ca2+ exchange in giant excised sarcolemmal membrane patches, Nature, 344, 242–245.

81. Hilgemann, D.W., Nicoll, D.A., and Philipson, K.D. (1991) Charge movement during Na+ translocation by native and cloned cardiac Na+/Ca2+ exchanger, Nature, 352, 715–718.

82. Sibarov, D.A., Abushik, P.A., Poguzhelskaya, E.E., Bolshakov, K.V., and Antonov, S.M. (2015) Inhibition of plasma membrane Na/Ca-exchanger by KB-R7943 or lithium reveals its role in Ca-dependent NMDAR inactivation, J. Pharmacol. Exp. Ther., 355, 484–495.

83. Sibarov, D.A., Bolshakov, A.E., Abushik, P.A., Krivoi, I.I., and Antonov, S.M. (2012) Na+,K+-ATPase functionally interacts with the plasma membrane Na+,Ca2+-exchanger to prevent Ca2+ overload and neuronal apoptosis in excito-toxic stress, J. Pharmacol. Exp. Ther., 343, 596–607.

84. Abushik, P.A., Sibarov, D.A., Eaton, M.J., Skatchkov, S.N., and Antonov, S.M. (2013) Kainate-induced calcium overload of cortical neurons in vitro: dependence on expression of AMPAR GluA2-subunit and down-regulation by subnanomolar ouabain, Cell Calcium, 54, 95–104.

85. Frank, C., Giammarioli, A.M., Pepponi, R., Fiorentini, C., and Rufini, S. (2004) Cholesterol perturbing agents inhibit NMDA-dependent calcium influx in rat hippocampal primary culture, FEBS Lett., 566, 25–29.

86. Korinek, M., Vyklicky, V., Borovska, J., Lichnerova, K., Kaniakova, M., Krausova, B., Krusek, J., Balik, A., Smejkalova, T., Horak, M., and Vyklicky, L. (2015) Cholesterol modulates open probability and desensitization of NMDA receptors, J. Physiol., 593, 2279–2293.

87. Abulrob, A., Tauskela, J.S., Mealing, G., Brunette, E., Faid, K., and Stanimirovic, D. (2005) Protection by cholesterol-extracting cyclodextrins: a role for N-methyl-D-aspartate receptor redistribution, J. Neurochem., 92, 1477–1486.

88. Besshoh, S., Chen, S., Brown, I.R., and Gurd, J.W. (2007) Developmental changes in the association of NMDA receptors with lipid rafts, J. Neurosci. Res., 85, 1876–1883.

89. Delinte-Ramirez, I., Salcedo-Tello, P., and Bermudez-Rattoni, F. (2008) Spatial memory formation induces recruitment of NMDA receptor and PSD-95 to synaptic lipid rafts, J. Neurochem., 106, 1658–1668.

90. Marques-da-Silva, D., and Gutierrez-Merino, C. (2012) L-type voltage-operated calcium channels, N-methyl-d-aspartate receptors and neuronal nitric-oxide synthase form a calcium/redox nano-transducer within lipid rafts, Biochem. Biophys. Res. Commun., 420, 257–262.

91. Marques-da-Silva, D., and Gutierrez-Merino, C. (2014) Caveolin-rich lipid rafts of the plasma membrane of mature cerebellar granule neurons are microcompartments for calcium/reactive oxygen and nitrogen species cross-talk signaling, Cell Calcium, 56, 108–123.

92. Pike, L.J. (2006) Rafts defined: a report on the keystone symposium on lipid rafts and cell function, J. Lipid Res., 47, 1597–1598.

93. Simons, M., Keller, P., De Strooper, B., Beyreuther, K., Dotti, C.G., and Simons, K. (1998) Cholesterol depletion inhibits the generation of beta-amyloid in hippocampal neurons, Proc. Natl. Acad. Sci. USA, 95, 6460–6464.

94. Wolf, A.A., Jobling, M.G., Wimer-Mackin, S., Ferguson-Maltzman, M., Madara, J.L., Holmes, R.K., Lencer, W.I., Ruston, S., Madara, J.L., and Hirst, T. (1998) Ganglioside structure dictates signal transduction by cholera toxin and association with caveolae-like membrane domains in polarized epithelia, J. Cell Biol., 141, 917–927.

95. Raghupathy, R., Anilkumar, A.A., Polley, A., Singh, P.P., Yadav, M., Johnson, C., Suryawanshi, S., Saikam, V., Sawant, S.D., Panda, A., Guo, Z., Vishwakarma, R.A., Rao, M., and Mayor, S. (2015) Transbilayer lipid interactions mediate nanoclustering of lipid-anchored proteins, Cell, 161, 581–594.

96. Iacobucci, G.J., and Popescu, G.K. (2017) Resident calmodulin primes NMDA receptors for Ca-dependent inactivation, Biophys. J., 113, 2236–2248.

97. Parekh, A.B. (2008) Ca2+ microdomains near plasma membrane Ca2+ channels: impact on cell function, J. Physiol., 586, 3043–3054.

98. Petersen, A., and Gerges, N.Z. (2015) Neurogranin regulates CaM dynamics at dendritic spines, Sci. Rep., 5, 11135.

99. Hoffman, L., Chandrasekar, A., Wang, X., Putkey, J.A., and Waxham, M.N. (2014) Neurogranin alters the structure and calcium binding properties of calmodulin, J. Biol. Chem., 289, 14644–14655.

100. Goldberg, J. H., Tamas, G., Aronov, D., and Yuste, R. (2003) Calcium microdomains in aspiny dendrites, Neuron, 40, 807–821.

101. Chard, P.S., Jordan, J., Marcuccilli, C.J., Miller, R.J., Leiden, J.M., Roos, R.P., and Ghadge, G.D. (1995) Regulation of excitatory transmission at hippocampal synapses by calbindin D28k, Proc. Nat. Acad. Sci. USA, 92, 5144–5148.

102. Ponce, J., de la Ossa, N. P., Hurtado, O., Millan, M., Arenillas, J. F., Davalos, A., and Gasull, T. (2008) Simvastatin reduces the association of NMDA receptors to lipid rafts: a cholesterol-mediated effect in neuroprotection, Stroke, 39, 1269–1275.

103. Valiullina, F., Zakharova, Y., Mukhtarov, M., Draguhn, A., Burnashev, N., and Rozov, A. (2016) The relative contribution of NMDARs to excitatory postsynaptic currents is controlled by Ca2+-induced inactivation, Front. Cell. Neurosci., 10, doi: 10.3389/fncel.2016.00012.

104. Frank, C., Rufini, S., Tancredi, V., Forcina, R., Grossi, D., and D’Arcangelo, G. (2008) Cholesterol depletion inhibits synaptic transmission and synaptic plasticity in rat hippocampus, Exp. Neurol., 212, 407–414.