NFAT-dependent gene expression in the nervous system: A critical mediator of neurotrophin-induced plasticity

Transcriptional Regulation by Neuronal Activity: To the Nucleus and Back

Volumn , Issue , 2008, Pages 187-208

  Groth, Rachel D ^a   Mermelstein, Paul G ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84861867390     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-0-387-73609-9_10     Document Type: Chapter

References (161)

1. Ahamed, J., Venkatesha, R. T., Thangam, E. B. and Ali, H. (2004) C3a enhances nerve growth factor-induced NFAT activation and chemokine production in a human mast cell line, HMC-1. J. Immunol. 172, 6961-6968.
2. Aloe, L., Tuveri, M. A. and Levi-Montalcini, R. (1992) Studies on carrageenan-induced arthritis in adult rats: presence of nerve growth factor and role of sympathetic innervation. Rheumatol. Int. 12, 213-216.
3. Andreev, N. Y., Dimitrieva, N., Koltzenburg, M. and McMahon, S. B. (1995) Peripheral administration of nerve growth factor in the adult rat produces a thermal hyperalgesia that requires the presence of sympathetic post-ganglionic neurones. Pain. 63, 109-115.
4. Apfel, S. C., Wright, D. E., Wiideman, A. M., Dormia, C., Snider, W. D. and Kessler, J. A. (1996) Nerve growth factor regulates the expression of brain-derived neurotrophic factor mRNA in the peripheral nervous system. Mol. Cell Neurosci. 7, 134-142.
5. Asai, M., Iwasaki, Y., Yoshida, M., Mutsuga-Nakayama, N., Arima, H., Ito, M., Takano, K. and Oiso, Y. (2004) Nuclear factor of activated T cells (NFAT) is involved in the depolarizationinduced activation of growth hormone-releasing hormone gene transcription in vitro. Mol. Endocrinol. 18, 3011-3019.
6. Ayer-LeLievre, C., Olson, L., Ebendal, T., Seiger, A. and Persson, H. (1988) Expression of the beta-nerve growth factor gene in hippocampal neurons. Science. 240, 1339-1341.
7. Baksh, S., Widlund, H. R., Frazer-Abel, A. A., Du, J., Fosmire, S., Fisher, D. E., DeCaprio, J. A., Modiano, J. F. and Burakoff, S. J. (2002) NFATc2-mediated repression of cyclin-dependent kinase 4 expression. Mol. Cell. 10, 1071-1081.
8. Barnes, C. A. (1979)Memory deficits associated with senescence: A neurophysiological and behavioral study in the rat. J. Comp. Physiol. Psychol.. 93, 74-104.
9. Beals, C. R., Sheridan, C. M., Turck, C.W., Gardner, P. and Crabtree, G. R. (1997) Nuclear export of NF-ATc enhanced by glycogen synthase kinase-3. Science. 275, 1930-1934.
10. Beiche, F., Brune, K., Geisslinger, G. and Goppelt-Struebe, M. (1998) Expression of cyclooxygenase isoforms in the rat spinal cord and their regulation during adjuvant-induced arthritis. Inflamm Res. 47, 482-487.
11. Benedito, A. B., Lehtinen, M., Massol, R., Lopes, U. G., Kirchhausen, T., Rao, A. and Bonni, A. (2005) The transcription factor NFAT3 mediates neuronal survival. J. Biol. Chem. 280, 2818-2825.
12. Bennett, G., al-Rashed, S., Hoult, J. R. and Brain, S. D. (1998) Nerve growth factor induced hyperalgesia in the rat hind paw is dependent on circulating neutrophils. Pain. 77, 315-322.
13. Bert, A. G., Burrows, J., Hawwari, A., Vadas, M. A. and Cockerill, P. N. (2000) Reconstitution of T cell-specific transcription directed by composite NFAT/Oct elements. J. Immunol. 165, 5646-5655.
14. Bodor, J., Bodorova, J. and Gress, R. E. (2000) Suppression of T cell function: A potential role for transcriptional repressor ICER. J. Leukoc. Biol. 67, 774-779.
15. Bonnington, J. K. and McNaughton, P. A. (2003) Signalling pathways involved in the sensitisation of mouse nociceptive neurones by nerve growth factor. J. Physiol. 551, 433-446.
16. Boss, V., Talpade, D. J. and Murphy, T. J. (1996) Induction of NFAT-mediated transcription by Gq-coupled receptors in lymphoid and non-lymphoid cells. J. Biol. Chem. 271, 10429-10432.
17. Bower, K. E., Zeller, R.W., Wachsman, W., Martinez, T. and McGuire, K. L. (2002) Correlation of transcriptional repression by p21(SNFT) with changes in DNA.NF-AT complex interactions. J. Biol. Chem. 277, 34967-34977.
18. Bradley, K. C., Groth, R. D. and Mermelstein, P. G. (2005) Immunolocalization of NFATc4 in the adult mouse brain. J. Neurosci. Res. 82, 762-770.
19. Castren, E., Pitkanen, M., Sirvio, J., Parsadanian, A., Lindholm, D., Thoenen, H. and Riekkinen, P. J. (1993) The induction of LTP increases BDNF and NGF mRNA but decreases NT-3 mRNA in the dentate gyrus. Neuroreport 4, 895-898.
20. Chen, L., Glover, J. N., Hogan, P. G., Rao, A. and Harrison, S. C. (1998) Structure of the DNAbinding domains from NFAT, Fos and Jun bound specifically to DNA. Nature 392, 42-48.
21. Chin, E. R., Olson, E. N., Richardson, J. A., Yang, Q., Humphries, C., Shelton, J. M., Wu, H., Zhu, W., Bassel-Duby, R. and Williams, R. S. (1998) A calcineurin-dependent transcriptional pathway controls skeletal muscle fiber type. Genes Dev. 12, 2499-2509.
22. Cho, H. J., Kim, S. Y., Park, M. J., Kim, D. S., Kim, J. K. and Chu, M. Y. (1997) Expression of mRNA for brain-derived neurotrophic factor in the dorsal root ganglion following peripheral inflammation. Brain Res. 749, 358-362.
23. Chow, C.W., Rincon, M., Cavanagh, J., Dickens, M. and Davis, R. J. (1997) Nuclear accumulation of NFAT4 opposed by the JNK signal transduction pathway. Science 278, 1638-1641.
24. Chytil, M. and Verdine, G. L. (1996) The Rel family of eukaryotic transcription factors. Curr. Opin. Struct. Biol. 6, 91-100.
25. Clipstone, N. A. and Crabtree, G. R. (1992) Identification of calcineurin as a key signalling enzyme in T-lymphocyte activation. Nature 357, 695-697.
26. Crabtree, G. R. and Olson, E. N. (2002) NFAT signaling: choreographing the social lives of cells. Cell 109 Suppl, S67-S79.
27. Cross, D. A., Alessi, D. R., Cohen, P., Andjelkovich, M. and Hemmings, B. A. (1995) Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378, 785-789.
28. de la Pompa, J. L., Timmerman, L. A., Takimoto, H., Yoshida, H., Elia, A. J., Samper, E., Potter, J., Wakeham, A., Marengere, L., Langille, B. L., Crabtree, G. R. and Mak, T. W. (1998) Role of the NF-ATc transcription factor in morphogenesis of cardiac valves and septum. Nature 392, 182-186.
29. Decker, E. L., Nehmann, N., Kampen, E., Eibel, H., Zipfel, P. F. and Skerka, C. (2003) Early growth response proteins (EGR) and nuclear factors of activated T cells (NFAT) form heterodimers and regulate proinflammatory cytokine gene expression. Nucleic Acids Res. 31, 911-921.
30. Decker, E. L., Skerka, C. and Zipfel, P. F. (1998) The early growth response protein (EGR-1) regulates interleukin-2 transcription by synergistic interaction with the nuclear factor of activated T cells. J. Biol. Chem. 273, 26923-26930.
31. Deisseroth, K., Mermelstein, P. G., Xia, H. and Tsien, R. W. (2003) Signaling from synapse to nucleus: The logic behind the mechanisms. Curr. Opin. Neurobiol. 13, 354-365.
32. Dolmetsch, R. (2003) Excitation-transcription coupling: Signaling by ion channels to the nucleus. Sci STKE. 2003, PE4.
33. Donnerer, J., Schuligoi, R. and Stein, C. (1992) Increased content and transport of substance P and calcitonin gene-related peptide in sensory nerves innervating inflamed tissue: evidence for a regulatory function of nerve growth factor in vivo. Neuroscience 49, 693-698.
34. Dragunow, M., Beilharz, E., Mason, B., Lawlor, P., Abraham, W. and Gluckman, P. (1993) Brain-derived neurotrophic factor expression after long-term potentiation. Neurosci. Lett. 160, 232-236.
35. Emmel, E. A., Verweij, C. L., Durand, D. B., Higgins, K. M., Lacy, E. and Crabtree, G. R. (1989) Cyclosporin A specifically inhibits function of nuclear proteins involved in T cell activation. Science 246, 1617-1620.
36. Ermak, G., Morgan, T. E. and Davies, K. J. (2001) Chronic overexpression of the calcineurin inhibitory gene DSCR1 (Adapt78) is associated with Alzheimer's disease. J. Biol. Chem. 276, 38787-38794.
37. Ernfors, P., Wetmore, C., Olson, L. and Persson, H. (1990) Identification of cells in rat brain and peripheral tissues expressing mRNA for members of the nerve growth factor family. Neuron 5, 511-526.
38. Figurov, A., Pozzo-Miller, L. D., Olafsson, P., Wang, T. and Lu, B. (1996) Regulation of synaptic responses to high-frequency stimulation and LTP by neurotrophins in the hippocampus. Nature 381, 706-709.
39. Finkbeiner, S. (2000) CREB couples neurotrophin signals to survival messages. Neuron 25, 11-14.
40. Flanagan, W. M., Corthesy, B., Bram, R. J. and Crabtree, G. R. (1991) Nuclear association of a T-cell transcription factor blocked by FK-506 and cyclosporin A. Nature 352, 803-807.
41. Foehr, E. D., Lin, X., O'Mahony, A., Geleziunas, R., Bradshaw, R. A. and Greene, W. C. (2000) NF-kappa B signaling promotes both cell survival and neurite process formation in nerve growth factor-stimulated PC12 cells. J. Neurosci. 20, 7556-7563.
42. Furstenau, U., Schwaninger, M., Blume, R., Jendrusch, E.M. and Knepel, W. (1999) Characterization of a novel calcium response element in the glucagon gene. J. Biol. Chem. 274, 5851-5860.
43. Genazzani, A. A., Carafoli, E. and Guerini, D. (1999) Calcineurin controls inositol 1, 4, 5- Trisphosphate type 1 receptor expression in neurons. Proc. Natl. Acad. Sci. USA. 96, 5797-5801.
44. Giffin, M. J., Stroud, J. C., Bates, D. L., von Koenig, K. D., Hardin, J. and Chen, L. (2003) Structure of NFAT1 bound as a dimer to the HIV-1 LTR kappa B element. Nat. Struct. Biol. 10, 800-806.
45. Ginty, D. D. and Segal, R. A. (2002) Retrograde neurotrophin signaling: Trk-ing along the axon. Curr. Opin. Neurobiol. 12, 268-274.
46. Gomez del Arco, P., Martinez-Martinez, S., Maldonado, J. L., Ortega-Perez, I. and Redondo, J. M. (2000) A role for the p38 MAP kinase pathway in the nuclear shuttling of NFATp. J. Biol. Chem. 275, 13872-13878.
47. Graef, I. A., Chen, F., Chen, L., Kuo, A. and Crabtree, G. R. (2001) Signals transduced by Ca(2+)/calcineurin and NFATc3/c4 pattern the developing vasculature. Cell 105, 863-875.
48. Graef, I. A., Mermelstein, P. G., Stankunas, K., Neilson, J. R., Deisseroth, K., Tsien, R. W. and Crabtree, G. R. (1999) L-type calcium channels and GSK-3 regulate the activity of NF-ATc4 in hippocampal neurons. Nature 401, 703-708.
49. Graef, I. A., Wang, F., Charron, F., Chen, L., Neilson, J., Tessier-Lavigne, M. and Crabtree, G. R. (2003) Neurotrophins and netrins require calcineurin/NFAT signaling to stimulate outgrowth of embryonic axons. Cell 113, 657-670.
50. Groth, R. and Aanonsen, L. (2002) Spinal brain-derived neurotrophic factor (BDNF) produces hyperalgesia in normal mice while antisense directed against either BDNF or trkB, prevent inflammation-induced hyperalgesia. Pain 100, 171-181.
51. Groth, R.D., Bradley, K.C., Mermelstein, P.G., Nakagawa, Y. (2006a) Expression of NFATc1-4 mRNA Within the Adult Mouse Brain. Submitted.
52. Groth RD, Coicou LG, Seybold VS (2006b) Neurotrophin Activation of NFAT-Dependent Transcription Within Primary Afferent and Spinal Neurons Contributes to Expression of Pro- Nociceptive Genes. Submitted.
53. Groth, R. D., Dunbar, R. L. and Mermelstein, P. G. (2003) Calcineurin regulation of neuronal plasticity. Biochem. Biophys. Res. Commun. 311, 1159-1171.
54. Groth, R. D. and Mermelstein, P. G. (2003) Brain-derived neurotrophic factor activation of NFAT (nuclear factor of activated T-cells)-dependent transcription: A role for the transcription factor NFATc4 in neurotrophin-mediated gene expression. J. Neurosci. 23, 8125-8134.
55. Hay, C. and de Belleroche, J. (1997) Carrageenan-induced hyperalgesia is associated with increased cyclo-oxygenase-2 expression in spinal cord. Neuroreport. 8, 1249-1251.
56. Ho, I. C., Kim, J. H., Rooney, J. W., Spiegelman, B. M. and Glimcher, L. H. (1998) A potential role for the nuclear factor of activated T cells family of transcriptional regulatory proteins in adipogenesis. Proc. Natl. Acad. Sci. USA. 95, 15537-15541.
57. Ho, I. C., Hodge, M. R., Rooney, J. W. and Glimcher, L. H. (1996) The proto-oncogene c-maf is responsible for tissue-specific expression of interleukin-4. Cell 85, 973-983.
58. Ho, S., Timmerman, L., Northrop, J. and Crabtree, G. R. (1994) Cloning and characterization of NF-ATc and NF-ATp: The cytoplasmic components of NF-AT. Adv. Exp. Med. Biol. 365, 167-173.
59. Hoey, T., Sun, Y. L., Williamson, K. and Xu, X. (1995) Isolation of two new members of the NF-AT gene family and functional characterization of the NF-AT proteins. Immunity. 2, 461-472.
60. Hofer, M., Pagliusi, S. R., Hohn, A., Leibrock, J. and Barde, Y. A. (1990) Regional distribution of brain-derived neurotrophic factor mRNA in the adult mouse brain. EMBO J. 9, 2459-2464.
61. Hogan, P. G., Chen, L., Nardone, J. and Rao, A. (2003) Transcriptional regulation by calcium, calcineurin, and NFAT. Genes Dev. 17, 2205-2232.
62. Holsinger, R. M., Schnarr, J., Henry, P., Castelo, V. T. and Fahnestock, M. (2000) Quantitation of BDNF mRNA in human parietal cortex by competitive reverse transcription-polymerase chain reaction: decreased levels in Alzheimer's disease. Brain Res. Mol. Brain Res. 76, 347-354.
63. Horigome, K., Bullock, E. D. and Johnson, E. M. J. (1994) Effects of nerve growth factor on rat peritoneal mast cells. Survival promotion and immediate-early gene induction. J. Biol. Chem. 269, 2695-2702.
64. Hu, C. M., Jang, S. Y., Fanzo, J. C. and Pernis, A. B. (2002) Modulation of T cell cytokine production by interferon regulatory factor-4. J. Biol. Chem. 277, 49238-49246.
65. Huang, E. J. and Reichardt, L. F. (2001) Neurotrophins: roles in neuronal development and function. Annu. Rev. Neurosci. 24, 677-736.
66. Huxford, T., Huang, D. B., Malek, S. and Ghosh, G. (1998) The crystal structure of the IkappaBalpha/NF-kappaB complex reveals mechanisms of NF-kappaB inactivation. Cell 95, 759-770.
67. Iniguez, M. A., Martinez-Martinez, S., Punzon, C., Redondo, J. M. and Fresno, M. (2000) An essential role of the nuclear factor of activated T cells in the regulation of the expression of the cyclooxygenase-2 gene in human T lymphocytes. J. Biol. Chem. 275, 23627-23635.
68. Isakov, N. and Altman, A. (2002) Protein kinase C(theta) in T cell activation. Annu. Rev. Immunol. 20, 761-794.
69. Jacobs, M. D. and Harrison, S. C. (1998) Structure of an IkappaBalpha/NF-kappaB complex. Cell 95, 749-758.
70. Jayanthi, S., Deng, X., Ladenheim, B., McCoy, M. T., Cluster, A., Cai, N. S. and Cadet, J. L. (2005) Calcineurin/NFAT-induced up-regulation of the Fas ligand/Fas death pathway is involved in methamphetamine-induced neuronal apoptosis. Proc. Natl. Acad. Sci. USA. 102, 868-873.
71. Jin, L., Sliz, P., Chen, L., Macian, F., Rao, A., Hogan, P. G. and Harrison, S. C. (2003) An asymmetric NFAT1 dimer on a pseudo-palindromic kappa B-like DNA site. Nat. Struct. Biol. 10, 807-811.
72. Kang, H. and Schuman, E. M. (1995) Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science 267, 1658-1662.
73. Kang, H. and Schuman, E. M. (1996) A requirement for local protein synthesis in neurotrophininduced hippocampal synaptic plasticity. Science 273, 1402-1406.
74. Kang, H., Welcher, A. A., Shelton, D. and Schuman, E. M. (1997) Neurotrophins and time: different roles for TrkB signaling in hippocampal long-term potentiation. Neuron 19, 653-664.
75. Kaplan, D. R., Martin-Zanca, D. and Parada, L. F. (1991) Tyrosine phosphorylation and tyrosine kinase activity of the trk proto-oncogene product induced by NGF. Nature 350, 158-160.
76. Kaplan, D. R. and Miller, F. D. (2000) Neurotrophin signal transduction in the nervous system. Curr. Opin. Neurobiol. 10, 381-391.
77. Kerr, B. J., Bradbury, E. J., Bennett, D. L., Trivedi, P. M., Dassan, P., French, J., Shelton, D. B., McMahon, S. B. and Thompson, S. W. (1999) Brain-derived neurotrophic factor modulates nociceptive sensory inputs and NMDA-evoked responses in the rat spinal cord. J. Neurosci. 19, 5138-5148.
78. Kincaid, R. L., Balaban, C. D. and Billingsley, M. L. (1987) Differential localization of calmodulindependent enzymes in rat brain: evidence for selective expression of cyclic nucleotide phosphodiesterase in specific neurons. Proc. Natl. Acad. Sci. USA. 84, 1118-1122.
79. Korte, M., Carroll, P., Wolf, E., Brem, G., Thoenen, H. and Bonhoeffer, T. (1995) Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc. Natl. Acad. Sci. USA. 92, 8856-8860.
80. Korte, M., Griesbeck, O., Gravel, C., Carroll, P., Staiger, V., Thoenen, H. and Bonhoeffer, T. (1996) Virus-mediated gene transfer into hippocampal CA1 region restores long-term potentiation in brain-derived neurotrophic factor mutant mice. Proc. Natl. Acad. Sci. USA. 93, 12547-12552.
81. Lamballe, F., Klein, R. and Barbacid, M. (1991) The trk family of oncogenes and neurotro phin receptors. Princess Takamatsu Symp. 22, 153-170.
82. Lever, I. J., Bradbury, E. J., Cunningham, J. R., Adelson, D. W., Jones, M. G., McMahon, S. B., Marvizon, J. C. and Malcangio, M. (2001) Brain-derived neurotrophic factor is released in the dorsal horn by distinctive patterns of afferent fiber stimulation. J. Neurosci. 21, 4469-4477.
83. Levine, E. S., Dreyfus, C. F., Black, I. B. and Plummer, M. R. (1995) Brain-derived neurotrophic factor rapidly enhances synaptic transmission in hippocampal neurons via postsynaptic tyrosine kinase receptors. Proc. Natl. Acad. Sci. USA. 92, 8074-8077.
84. Liu, J., Farmer, J. D. J., Lane, W. S., Friedman, J., Weissman, I. and Schreiber, S. L. (1991) Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell 66, 807-815.
85. Liu, Q. R., Lu, L., Zhu, X. G., Gong, J. P., Shaham, Y. and Uhl, G. R. (2006) Rodent BDNF genes, novel promoters, novel splice variants, and regulation by cocaine. Brain Res. 1067, 1-12.
86. Lonze, B. E., Riccio, A., Cohen, S. and Ginty, D. D. (2002) Apoptosis, axonal growth defects, and degeneration of peripheral neurons in mice lacking CREB. Neuron 34, 371-385.
87. Lopez-Rodriguez, C., Aramburu, J., Rakeman, A. S. and Rao, A. (1999) NFAT5, a constitutively nuclear NFAT protein that does not cooperate with Fos and Jun. Proc. Natl. Acad. Sci. USA. 96, 7214-7219.
88. Macian, F., Garcia-Rodriguez, C. and Rao, A. (2000) Gene expression elicited by NFAT in the presence or absence of cooperative recruitment of Fos and Jun. EMBO J. 19, 4783-4795.
89. Macian, F., Lopez-Rodriguez, C. and Rao, A. (2001) Partners in transcription: NFAT and AP-1. Oncogene. 20, 2476-2489.
90. Mannion, R. J., Costigan, M., Decosterd, I., Amaya, F., Ma, Q. P., Holstege, J. C., Ji, R. R., Acheson, A., Lindsay, R. M., Wilkinson, G. A. and Woolf, C. J. (1999) Neurotrophins: peripherally and centrally acting modulators of tactile stimulus-induced inflammatory pain hypersensitivity. Proc. Natl. Acad. Sci. USA. 96, 9385-9390.
91. Mao, Z., Bonni, A., Xia, F., Nadal-Vicens, M. and Greenberg, M. E. (1999) Neuronal activitydependent cell survival mediated by transcription factor MEF2. Science. 286, 785-790.
92. Markus, A., Patel, T. D. and Snider, W. D. (2002) Neurotrophic factors and axonal growth. Curr. Opin. Neurobiol. 12, 523-531.
93. Mazurek, N., Weskamp, G., Erne, P. and Otten, U. (1986) Nerve growth factor induces mast cell degranulation without changing intracellular calcium levels. FEBS Lett. 198, 315-320.
94. McKinsey, T. A., Zhang, C. L. and Olson, E. N. (2002) MEF2: A calcium-dependent regulator of cell division, differentiation and death. Trends Biochem. Sci. 27, 40-47.
95. Mendell, L. M., Albers, K. M. and Davis, B. M. (1999) Neurotrophins, nociceptors, and pain. Microsc. Res. Tech. 45, 252-261.
96. Michael, G. J., Averill, S., Nitkunan, A., Rattray, M., Bennett, D. L., Yan, Q. and Priestley, J. V. (1997) Nerve growth factor treatment increases brain-derived neurotrophic factor selectively in TrkA-expressing dorsal root ganglion cells and in their central terminations within the spinal cord. J. Neurosci. 17, 8476-8490.
97. Millan, M. J. (1999) The induction of pain: An integrative review. Prog. Neurobiol. 57, 1-164.
98. Miller, F. D. and Kaplan, D. R. (2001) On Trk for retrograde signaling. Neuron 32, 767-770.
99. Minichiello, L., Calella, A. M., Medina, D. L., Bonhoeffer, T., Klein, R. and Korte, M. (2002) Mechanism of TrkB-mediated hippocampal long-term potentiation. Neuron 36, 121-137.
100. Misra, R. P., Bonni, A., Miranti, C. K., Rivera, V. M., Sheng, M. and Greenberg, M. E. (1994) L-type voltage-sensitive calcium channel activation stimulates gene expression by a serum response factor-dependent pathway. J. Biol. Chem. 269, 25483-25493.
101. Miyakawa, H., Woo, S. K., Dahl, S. C., Handler, J. S. and Kwon, H.M. (1999) Tonicity-responsive enhancer binding protein, a rel-like protein that stimulates transcription in response to hypertonicity. Proc. Natl. Acad. Sci. USA. 96, 2538-2542.
102. Molkentin, J. D., Lu, J. R., Antos, C. L., Markham, B., Richardson, J., Robbins, J., Grant, S. R. and Olson, E. N. (1998) A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell 93, 215-228.
103. Murer, M. G., Yan, Q. and Raisman-Vozari, R. (2001) Brain-derived neurotrophic factor in the control human brain, and in Alzheimer's disease and Parkinson's disease. Prog. Neurobiol. 63, 71-124.
104. Myers, S. J., Peters, J., Huang, Y., Comer, M. B., Barthel, F. and Dingledine, R. (1998) Transcriptional regulation of the GluR2 gene: neural-specific expression, multiple promoters, and regulatory elements. J. Neurosci. 18, 6723-6739.
105. Northrop, J. P., Ho, S. N., Chen, L., Thomas, D. J., Timmerman, L. A., Nolan, G. P., Admon, A. and Crabtree, G. R. (1994) NF-AT components define a family of transcription factors targeted in T-cell activation. Nature 369, 497-502.
106. Obermeier, A., Lammers, R., Wiesmuller, K. H., Jung, G., Schlessinger, J. and Ullrich, A. (1993) Identification of Trk binding sites for SHC and phosphatidylinositol 3'-kinase and formation of a multimeric signaling complex. J. Biol. Chem. 268, 22963-22966.
107. Ohmichi, M., Decker, S. J. and Saltiel, A. R. (1992b) Activation of phosphatidylinositol-3 kinase by nerve growth factor involves indirect coupling of the trk proto-oncogene with src homology 2 domains. Neuron 9, 769-777.
108. Ohmichi, M., Decker, S. J. and Saltiel, A. R. (1992a) Nerve growth factor stimulates the tyrosine phosphorylation of a 38-kDa protein that specifically associates with the src homology domain of phospholipase C-gamma 1. J. Biol. Chem. 267, 21601-21606.
109. Olson, E. N. and Williams, R. S. (2000) Remodeling muscles with calcineurin. Bioessays 22, 510-519.
110. Pap, M. and Cooper, G. M. (1998) Role of glycogen synthase kinase-3 in the phosphatidylinositol 3-Kinase/Akt cell survival pathway. J. Biol. Chem. 273, 19929-19932.
111. Patel, T. D., Jackman, A., Rice, F. L., Kucera, J. and Snider, W. D. (2000) Development of sensory neurons in the absence of NGF/TrkA signaling in vivo. Neuron 25, 345-357.
112. Patterson, S. L., Abel, T., Deuel, T. A., Martin, K. C., Rose, J. C. and Kandel, E. R. (1996) Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice. Neuron 16, 1137-1145.
113. Patterson, S. L., Grover, L.M., Schwartzkroin, P. A. and Bothwell, M. (1992) Neurotrophin expression in rat hippocampal slices: A stimulus paradigm inducing LTP in CA1 evokes increases in BDNF and NT-3 mRNAs. Neuron 9, 1081-1088.
114. Phillips, H. S., Hains, J. M., Armanini, M., Laramee, G. R., Johnson, S. A. and Winslow, J. W. (1991) BDNF mRNA is decreased in the hippocampus of individuals with Alzheimer's disease. Neuron 7, 695-702.
115. Plyte, S., Boncristiano, M., Fattori, E., Galvagni, F., Paccani, S. R., Majolini, M. B., Oliviero, S., Ciliberto, G., Telford, J. L. and Baldari, C. T. (2001) Identification and characterization of a novel nuclear factor of activated T-cells-1 isoform expressed in mouse brain. J. Biol. Chem. 276, 14350-14358.
116. Polli, J. W., Billingsley, M. L. and Kincaid, R. L. (1991) Expression of the calmodulin-dependent protein phosphatase, calcineurin, in rat brain: developmental patterns and the role of nigrostriatal innervation. Brain Res. Dev. Brain Res. 63, 105-119.
117. Ranger, A. M., Gerstenfeld, L. C., Wang, J., Kon, T., Bae, H., Gravallese, E. M., Glimcher, M. J. and Glimcher, L. H. (2000) The nuclear factor of activated T cells (NFAT) transcription factor NFATp (NFATc2) is a repressor of chondrogenesis. J. Exp. Med. 191, 9-22.
118. Ranger, A. M., Grusby, M. J., Hodge, M. R., Gravallese, E. M., de la Brousse, F. C., Hoey, T., Mickanin, C., Baldwin, H. S. and Glimcher, L. H. (1998) The transcription factor NF-ATc is essential for cardiac valve formation. Nature 392, 186-190.
119. Rao, A., Luo, C. and Hogan, P. G. (1997) Transcription factors of the NFAT family: regulation and function. Annu. Rev. Immunol. 15, 707-747.
120. Rengarajan, J., Mowen, K. A., McBride, K. D., Smith, E. D., Singh, H. and Glimcher, L. H. (2002) Interferon regulatory factor 4 (IRF4) interacts with NFATc2 to modulate interleukin 4 gene expression. J. Exp. Med. 195, 1003-1012.
121. Reynolds, A. J., Bartlett, S. E. and Hendry, I. A. (2000) Molecular mechanisms regulating the retrograde axonal transport of neurotrophins. Brain Res. Brain Res. Rev. 33, 169-178.
122. Riccio, A., Ahn, S., Davenport, C. M., Blendy, J. A. and Ginty, D. D. (1999) Mediation by a CREB family transcription factor of NGF-dependent survival of sympathetic neurons. Science 286, 2358-2361.
123. Rothermel, B. A., Vega, R. B. and Williams, R. S. (2003) The role of modulatory calcineurininteracting proteins in calcineurin signaling. Trends Cardiovasc. Med. 13, 15-21.
124. Saarelainen, T., Vaittinen, S. and Castren, E. (2001) trkB-receptor activation contributes to the kainate-induced increase in BDNF mRNA synthesis. Cell. Mol. Neurobiol. 21, 429-435.
125. Samad, T. A., Moore, K. A., Sapirstein, A., Billet, S., Allchorne, A., Poole, S., Bonventre, J. V. and Woolf, C. J. (2001) Interleukin-1beta-mediated induction of Cox-2 in the CNS contributes to inflammatory pain hypersensitivity. Nature. 410, 471-475.
126. Schreiber, S. L. and Crabtree, G. R. (1995) Immunophilins, ligands, and the control of signal transduction. Harvey Lect. 91, 99-114.
127. Seybold, V. S., Coicou, L. G., Groth, R. D. and Mermelstein, P. G. (2006) Substance P initiates NFAT-dependent gene expression in spinal neurons. J. Neurochem. 97, 397-407.
128. Seybold, V. S., Jia, Y. P. and Abrahams, L. G. (2003) Cyclo-oxygenase-2 contributes to central sensitization in rats with peripheral inflammation. Pain 105, 47-55.
129. Shaw, J. P., Utz, P. J., Durand, D. B., Toole, J. J., Emmel, E. A. and Crabtree, G. R. (1988) Identification of a putative regulator of early T cell activation genes. Science 241, 202-205.
130. Shen, W., Zhang, C. and Zhang, G. (2002) Nuclear factor kappaB activation is mediated by NMDA and non-NMDA receptor and L-type voltage-gated Ca(2+) channel following severe global ischemia in rat hippocampus. Brain Res. 933, 23-30.
131. Shieh, P. B., Hu, S. C., Bobb, K., Timmusk, T. and Ghosh, A. (1998) Identification of a signaling pathway involved in calcium regulation of BDNF expression. Neuron 20, 727-740.
132. Shioda, N., Moriguchi, S., Shirasaki, Y. and Fukunaga, K. (2006) Generation of constitutively active calcineurin by calpain contributes to delayed neuronal death following mouse brain ischemia. J. Neurochem. 98, 310-320.
133. Shu, X. and Mendell, L. M. (1999) Nerve growth factor acutely sensitizes the response of adult rat sensory neurons to capsaicin. Neurosci. Lett. 274, 159-162.
134. Sofroniew, M. V., Howe, C. L. and Mobley, W. C. (2001) Nerve growth factor signaling, neuroprotection, and neural repair. Annu. Rev. Neurosci. 24, 1217-1281.
135. Soppet, D., Escandon, E., Maragos, J., Middlemas, D. S., Reid, S. W., Blair, J., Burton, L. E., Stanton, B. R., Kaplan, D. R., Hunter, T. and et, al. (1991) The neurotrophic factors brainderived neurotrophic factor and neurotrophin-3 are ligands for the trkB tyrosine kinase receptor. Cell 65, 895-903.
136. Stephens, R.M., Loeb, D.M., Copeland, T. D., Pawson, T., Greene, L. A. and Kaplan, D. R. (1994) Trk receptors use redundant signal transduction pathways involving SHC and PLC-gamma 1 to mediate NGF responses. Neuron 12, 691-705.
137. Tabakman, R., Lecht, S., Sephanova, S., Arien-Zakay, H. and Lazarovici, P. (2004) Interactions between the cells of the immune and nervous system: neurotrophins as neuroprotection mediators in CNS injury. Prog. Brain Res. 146, 387-401.
138. Takaishi, T., Saito, N., Kuno, T. and Tanaka, C. (1991) Differential distribution of the mRNA encoding two isoforms of the catalytic subunit of calcineurin in the rat brain. Biochem. Biophys. Res. Commun. 174, 393-398.
139. Tolwani, R. J., Buckmaster, P. S., Varma, S., Cosgaya, J. M., Wu, Y., Suri, C. and Shooter, E. M. (2002) BDNF overexpression increases dendrite complexity in hippocampal dentate gyrus. Neuroscience. 114, 795-805.
140. Tomita, M., Reinhold, M. I., Molkentin, J. D. and Naski, M. C. (2002) Calcineurin and NFAT4 induce chondrogenesis. J. Biol. Chem. 277, 42214-42218.
141. Tucker, K. L., Meyer, M. and Barde, Y. A. (2001) Neurotrophins are required for nerve growth during development. Nat. Neurosci. 4, 29-37.
142. Tyler, W. J. and Pozzo-Miller, L. D. (2001) BDNF enhances quantal neurotransmitter release and increases the number of docked vesicles at the active zones of hippocampal excitatory synapses. J. Neurosci. 21, 4249-4258.
143. Ueda, Y., Hirai, S., Osada, S., Suzuki, A., Mizuno, K. and Ohno, S. (1996) Protein kinase C activates the MEK-ERK pathway in a manner independent of Ras and dependent on Raf. J. Biol. Chem. 271, 23512-23519.
144. van Rooij, E., Doevendans, P. A., de Theije, C. C., Babiker, F. A., Molkentin, J. D. and de Windt, L. J. (2002) Requirement of nuclear factor of activated T-cells in calcineurinmediated cardiomyocyte hypertrophy. J. Biol. Chem. 277, 48617-48626.
145. Vetter, M. L., Martin-Zanca, D., Parada, L. F., Bishop, J. M. and Kaplan, D. R. (1991) Nerve growth factor rapidly stimulates tyrosine phosphorylation of phospholipase C-gamma 1 by a kinase activity associated with the product of the trk protooncogene. Proc. Natl. Acad. Sci. USA. 88, 5650-5654.
146. Weick, J. P., Groth, R. D., Isaksen, A. L. and Mermelstein, P. G. (2003) Interactions with PDZ proteins are required for L-type calcium channels to activate cAMP response element-binding protein-dependent gene expression. J. Neurosci. 23, 3446-3456.
147. Weick, J. P., Kuo, S. P. and Mermelstein, P. G. (2005a) L-type calcium channel regulation of neuronal gene expression. Cellsci. Rev. 1, 44-49.
148. Weick, J. P., Kuo, S. P. and Mermelstein, P. G. (2005b) NFATc regulates GluR2 expression in the hippocampus. Soc. Neurosci. Abstr. 734.14.
149. Weskamp, G. and Otten, U. (1987) An enzyme-linked immunoassay for nerve growth factor (NGF): A tool for studying regulatory mechanisms involved in NGF production in brain and in peripheral tissues. J. Neurochem. 48, 1779-1786.
150. West, A. E., Griffith, E. C. and Greenberg, M. E. (2002) Regulation of transcription factors by neuronal activity. Nat. Rev. Neurosci. 3, 921-931.
151. Woo, S. K., Lee, S. D. and Kwon, H. M. (2002) TonEBP transcriptional activator in the cellular response to increased osmolality. Pflugers Arch. 444, 579-585.
152. Woolf, C. J., Safieh-Garabedian, B., Ma, Q. P., Crilly, P. and Winter, J. (1994) Nerve growth factor contributes to the generation of inflammatory sensory hypersensitivity. Neuroscience. 62, 327-331.
153. Wooten, M.W., Seibenhener, M. L., Mamidipudi, V., Diaz-Meco, M. T., Barker, P. A. and Moscat, J. (2001) The atypical protein kinase C-interacting protein p62 is a scaffold for NF-kappaB activation by nerve growth factor. J. Biol. Chem. 276, 7709-7712.
154. Yang, J., Rothermel, B., Vega, R. B., Frey, N., McKinsey, T. A., Olson, E. N., Bassel-Duby, R. and Williams, R. S. (2000a) Independent signals control expression of the calcineurin inhibitory proteins MCIP1 and MCIP2 in striated muscles. Circ. Res. 87, E61-8.
155. Yang, T. T., Xiong, Q., Enslen, H., Davis, R. J. and Chow, C.W. (2002) Phosphorylation of NFATc4 by p38 mitogen-activated protein kinases. Mol. Cell Biol. 22, 3892-3904.
156. Yang, X. Y., Wang, L. H., Chen, T., Hodge, D. R., Resau, J. H., DaSilva, L. and Farrar, W. L. (2000b) Activation of human T lymphocytes is inhibited by peroxisome proliferator-activated receptor gamma (PPARgamma) agonists. PPARgamma co-association with transcription factor NFAT. J. Biol. Chem. 275, 4541-4544.
157. Yiu, G. K. and Toker, A. (2006) NFAT induces breast cancer cell invasion by promoting the induction of cyclooxygenase-2. J. Biol. Chem. 281, 12210-12217.
158. Yoshida, T. and Mishina, M. (2005) Distinct roles of calcineurin-nuclear factor of activated Tcells and protein kinase A-cAMP response element-binding protein signaling in presynaptic differentiation. J. Neurosci. 25, 3067-3079.
159. Zhang, H., Maximov, A., Fu, Y., Xu, F., Tang, T. S., Tkatch, T., Surmeier, D. J. and Bezprozvanny, I. (2005) Association of CaV1.3 L-type calcium channels with Shank. J. Neurosci. 25, 1037-1049.
160. Zhu, J., Shibasaki, F., Price, R., Guillemot, J. C., Yano, T., Dotsch, V., Wagner, G., Ferrara, P. and McKeon, F. (1998) Intramolecular masking of nuclear import signal on NF-AT4 by casein kinase I and MEKK1. Cell 93, 851-861.
161. Zhuang, Z. Y., Xu, H., Clapham, D. E. and Ji, R. R. (2004) Phosphatidylinositol 3-kinase activates ERK in primary sensory neurons and mediates inflammatory heat hyperalgesia through TRPV1 sensitization. J. Neurosci. 24, 8300-8309.